Perspectives in Astrobiology (NATO Science Series: Life and Behavioural Sciences, Vol. 366)

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Author: Richard B. Hoover | Aleksei Iurevich Rozanov | Roland Paepe

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PERSPECTIVES IN ASTROBIOLOGY

NATO Science Series A series presenting the results of scientific meetings supported under the NATO Science Programme. The series is published by IOS Press and Springer Science and Business Media in conjunction with the NATO Public Diplomacy Division. Sub-Series I. II. III. IV. V.

Life and Behavioural Sciences Mathematics, Physics and Chemistry Computer and Systems Sciences Earth and Environmental Sciences Science and Technology Policy

IOS Press Springer Science and Business Media IOS Press Springer Science and Business Media IOS Press

The NATO Science Series continues the series of books published formerly as the NATO ASI Series. The NATO Science Programme offers support for collaboration in civil science between scientists of countries of the Euro-Atlantic Partnership Council. The types of scientific meeting generally supported are “Advanced Study Institutes” and “Advanced Research Workshops”, although other types of meeting are supported from time to time. The NATO Science Series collects together the results of these meetings. The meetings are co-organized by scientists from NATO countries and scientists from NATO’s Partner countries – countries of the CIS and Central and Eastern Europe. Advanced Study Institutes are high-level tutorial courses offering in-depth study of latest advances in a field. Advanced Research Workshops are expert meetings aimed at critical assessment of a field, and identification of directions for future action. As a consequence of the restructuring of the NATO Science Programme in 1999, the NATO Science Series has been re-organized and there are currently five sub-series as noted above. Please consult the following web sites for information on previous volumes published in the series, as well as details of earlier sub-series: http://www.nato.int/science http://www.springeronline.nl http://www.iospress.nl http://www.wtv-books.de/nato_pco.htm

Series I: Life and Behavioural Sciences - Vol. 366

ISSN: 1566-7693

Perspectives in Astrobiology

Edited by

R.B. Hoover Space Science Department/SD50, NASA George C. Marshall Space Flight Center, Huntsville, AL, USA

A.Yu. Rozanov Paleontological Institute RAS, Moscow, Russia

and

R. Paepe GEOBOUND INTERNATIONAL Research Center & Free University of Brussels, Belgium

Amsterdam • Berlin • Oxford • Tokyo • Washington, DC Published in cooperation with NATO Public Diplomacy Division

Proceedings of the NATO Advanced Study Institute on Perspectives in Astrobiology Chania, Crete, Greece 7–16 October 2002

© 2005 IOS Press. All rights reserved. No part of this book may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, without prior written permission from the publisher. ISBN 1-58603-512-6 Library of Congress Control Number: 2005925127 Publisher IOS Press Nieuwe Hemweg 6B 1013 BG Amsterdam Netherlands fax: +31 20 620 3419 e-mail: [email protected] Distributor in the UK and Ireland IOS Press/Lavis Marketing 73 Lime Walk Headington Oxford OX3 7AD England fax: +44 1865 750079

Distributor in the USA and Canada IOS Press, Inc. 4502 Rachael Manor Drive Fairfax, VA 22032 USA fax: +1 703 323 3668 e-mail: [email protected]

LEGAL NOTICE The publisher is not responsible for the use which might be made of the following information. PRINTED IN THE NETHERLANDS

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Perspectives in Astrobiology R.B. Hoover et al. (Eds.) IOS Press, 2005 © 2005 IOS Press. All rights reserved.

Preface Astrobiology is the multi-disciplinary field devoted to the investigation of the origin; physical, chemical and environmental limitations; and the distribution in space and time of life on Earth and in the Cosmos. Astrobiology seeks an answer to one of the most fundamental of all questions: — Is Life Restricted to Planet Earth or is Life a Cosmic Imperative? Understanding the characteristics, properties, habits, and diversity of living organisms on Earth is crucial to determining where and how to search for evidence of life elsewhere. New techniques and methodologies must be developed in order to determine a suitable suite of valid biomarkers that is needed to facilitate the differentiation of abiotic processes from true signatures of life. This is crucial to establishing the criteria needed to properly evaluate potential biosignatures in ancient Earth rocks and in a wide variety of Astromaterials (e.g., meteorites, interstellar dust particles and samples returned from future space flight missions to comets, asteroids and Mars). It is well known that microbial extremophiles (e.g., prokaryotes such as archaea and bacteria) were the first life forms to appear on Earth. They are also the most abundant and the most widely distributed life forms on our planet. Extremophiles inhabit deep ice, deep crustal rocks, hydrothermal vents, permafrost and the deepest layers of the Antarctic Ice Sheet, deep marine sediments, acidic brines and hypersaline, alkaline lakes and lagoons. They live in the most hostile environments of our planet, growing wherever there is a source of water, energy, and carbon compounds and represent good analogs for life forms that may be present elsewhere in the Solar System Their life processes result in the production of biominerals, chiral amino acids, biological fractionation of stable isotopes, macromolecular fossils, chemical biosignatures and microfossils. This “Perspectives in Astrobiology” volume includes papers treating a wide variety of these topics. They range from considerations of relict microbial communities of extreme environments (e.g. hydrotherms, hypersaline lagoons, and soda lakes and the subglacial Antarctic ice sheet) to complex organic molecules such as sugars under prebiotic conditions, biominerals and biotic and abiotic framboidal microstructures in Earth rocks, the processes of mineralization and fossilization of cyanobacteria, and biomarkers and microfossils detected in carbonaceous meteorites. Other papers discuss the use of stable isotopes and their biological fractionation as a baseline for evaluating extraterrestrial evidence and the use of chirality and composition of indigenous amino acids for differentiating between terrestrial and extraterrestrial organic matter in Astromaterials. Also treated in this volume are geomorph parallels, sediment patterns, and cyclicities in permafrost sediments of Earth and Mars; the survival of bacteria in space, eclipsing binaries, and advanced DNA and protein chip technology for future robotic missions to search for life in the Solar System. Richard B. Hoover Alexei Yu. Rozanov Roland Paepe

vi

Acknowledgements The Director Mr. Richard B. HOOVER, Astrobiology Group Leader at the Space Science Department/SD50, NASA George C. Marshall Space Flight Center, Huntsville, AL 35812, USA, the first Co-director Professor Alexei Rozanov, Palaeontological Institute of the Russian Academy of Sciences, 117997, Profsoyuznaya St., 123, Moscow, Russia, and the second Co-director Professor Roland Paepe, GEOBOUND INTERNATIONAL and the Vrije Universiteit Brussel, Belgium, like to thank everybody who contributed to the success of this very first NATO-ASI meeting dealing with the topic on “Perspectives in Astrobiology”. When it was presented to NATO, it was received with great enthusiasm by Dr. Walter Kaffenberger, Director of the NATO Scientific Affairs Division for which reason we want to thank him here in the first place. In the second place we feel greatly indebted for his renewed efforts inside the NATO Administration for allocating an exceptionally second funding after the first meeting was cancelled as a result of the September 11th event in 2001. So, exactly one year later, in October 2002, the second attempt to hold the meeting at the Creta Paradise Hotel in Hania, Crete, became possible again and successful. Also the managers of this hotel have been extremely understanding with reservations made for the first year and transferring these payments to the second year thus enabling the meeting to continue in 2002. NASA provided most of the funding for long and expensive traveling from the USA, especially from cities along the West Coast as well as for the establishment of the excellent website through which all registrations could easily and effectively be made and announcements and changes with regard to the programme and hotel accommodations could rapidly be dispatched. With this respect, a special tribute is hereby made to honour all efforts made by Mr. Ronald Koczor of NASA George C. Marshall Space Flight Center, Huntsville, AL 35812, USA as well as for taking up the thankless task of reviewing session papers with the Director of this NATO ASI. Special grants were provided by INTAS for participants originating from Russia and countries incorporated in the former Union of Socialist Soviet Republics. We are extremely grateful to Dr. Ingmar Schmidt of INTAS for helping the NATO ASI organizational committee with INTAS funding despite considerable problems that were also raised here further to the postponement of the meeting. Sponsoring by GEOBOUND INTERNATIONAL allowed traveling for Europeans and greatly facilitated logistics before, during and after the meeting. The considerable efforts made in this field by Dr. Elfi Van Overloop, Research Associate of GEOBOUND INTERNATIONAL and permanent contact person with the NATO Administration, contributed highly to the success of the smoothly running local organization as expressed by the Director of the NATO ASI in his final address. To all Greek Colleagues from the Technical University of Crete, especially to Professor Theodore Markopoulos, Head of the Geology Department and honorable host of the most southern part in Europe, we feel very thankful for their technical and moral support, for the organization of the field excursions, and not the least, for giving linguistically assistance throughout the congress. Finally we are most grateful to Wilhelmina Muhs, GEOBOUND INTERNATIONAL associate, for taking up the technical production of this book with IOS and serving as an intermediate between the publisher and NASA.

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NATO Participants Name

Country

e-mail

Hoover, Richard Paepe, Roland Rozanov, Alexei

Directors and Staff USA Belgium Russia

[email protected] [email protected] [email protected]

Koczor, Ronald Overloop, Elfi van

USA Belgium

[email protected] [email protected]

Duve, Christian de Horneck, Gerda Ivanov, Mikhail McKay, David Perez-Mercator, Juan Schidlowski, Manfred Vorobyova, Lena Yushkin, Nikolai Zavarzin, Georgy

Lecturers Belgium Germany Russia USA Spain Germany Russia Russia Russia

[email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected]

viii

List of Student Participants Name

Starting Point

e-mail

Armstrong, John Huber, Julie Kaye, Jonathan Kolb, Vera Perry, Randall Schrenk, Matthew Turnbull, Margaret Wells, Llyd

USA Seattle, Washington Seattle, Washington Seattle, Washington Kenosha, Wisconsin Seattle, Washington Seattle, Washington Tucson, Arizona Seattle, Washington

[email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected]

RUSSIA & adjacent countries Astafieva, Marina Moscow Gerasimenko, Ludmilla Moscow Simakov, Michael Sint Petersburg Simakova, Yulya Moscow Ushatinskaya, Galina Moscow Serozhkin, Yuri Kiev, Ukraine Plotnikova, Liudmila Kiev, Ukraine Nemliher, Yuriy Tallinn, Estonia Omarov, Bigalievich Almaty, Kazahkstan Kruchek, Semen Minsk, Bielorussia

Andras, Sik Blazquez, Jesus Bonaccorsi, Rosalba Çiçek, Caner Erdem, Ahmet Gomez Gomez, Jose Gutierrez, Jordi Rettberg, Petra Tamas, Simon Toporski, Jan

EUROPE & Turkey Budapest Madrid, Spain Trieste, Italy Canakkale Canakkale Madrid Barcelona Koln, Germany Budapest Portsmouth, UK

[email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected]

[email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected] [email protected]

ix

1. SCHRENK Matthew, 2. NEMLIHER Yuri, 3. SIK Andreas, 4. ARMSTRONG John, 5. KOCZOR Ronald, 6. ENGEL Michael, 7. SERUSHKIN Yuri, 8. TOPORSKI Jan, 9. BLASQUEZ Jesus, 10. MCKAY David, 11. ZAVARZIN Georgiu, 12. ÇIÇEK Caner, 13. KAYE Jonathan, 14. SIMAKOV Michael, 15. RETTEBERG Petra, 16. MARKOPOULOS Theodoros, 17. PERRY Randall, 18. PEREZ-MERCADER Juan, 19. ROZANOV Alexei, 20. GUTIERREZ Jordi, 21. OMAROV Bigaliev, 22. KOLB Vera, 23. HUBER Julie, 24. TURNBULL Margaret, 25. HOOVER Richard, 26. YUSHKIN Nicolai, 27. ASTAFIEVA Marina, 28. HORNECK Gerda, 29. BONACCORSI Rosalba, 30. USHATINSKAYA Galina, 31. PAEPE Roland, 32. VAN OVERLOOP Elfi, 33. SCHIDLOWSKI Manfred, 34. GERASIMENKO Ludmila, 35. SIMAKOVA Yulia.

x

xi

Contents Preface Richard B. Hoover, Alexei Yu. Rozanov and Roland Paepe

v

Acknowledgements

vi

NATO Participants

vii

List of Student Participants

viii

Nature of Framboidal Structures in Black Shales (the Cambrian of the Siberian Platform and the Permian of the Barents Sea Shelf) Marina M. Astafieva

1

Bacteriomorphic Structures from the Sinsk Formation (Lower Cambrian of the Siberian Platform) Marina M. Astafieva

6

Constraining Subglacial Settings Using Clay-Supported Ice Rafted Detritus (Mud Grains) in Antarctic Marine Sediment: A Framework for Astrobiology Rosalba Bonaccorsi, Antonio Brambati, Lloyd H. Burckle and Alexander M. Piotrowski

11

Apsidal Motion Problem in the Eclipsing Binary Star DR Vulpeculae Caner Çiçek

21

Amino Acids: Probes for Life’s Origin in the Solar System Michael H. Engel, Vlad E. Andrus and Stephen A. Macko

25

Mineralization of Cyanobacteria L. Gerasimenko, V. Orleansky and L. Zaitseva

38

Microfossils, Biominerals, and Chemical Biomarkers in Meteorites Richard B. Hoover

43

Survival of Microorganisms in Space, an Experimental Contribution to the Discussion on Viable Transfer of Life in the Solar System Gerda Horneck

66

Reactions of Urazole and its Analogs with Sugars and Metals under Prebiotic Conditions Vera M. Kolb, Patricia A. Colloton and Kevin J. Rapp

76

Apatite as Biosignature Jüri Nemliher

81

xii

Tikhov’s Astrobotany as a Prelude to Modern Astrobiology Tuken B. Omarov and Bulat T. Tashenov

86

Computation of Sediment Cycles on Mars and Earth Elfi Van Overloop and Roland Paepe

88

Landscape, Sediment, Red Soil, Permafrost Geomorph Parallels on Earth and Mars Roland Paepe and Elfi Van Overloop

104

Biochemical Markers in Rock Coatings Randall S. Perry and Vera M. Kolb

120

The Influence of Space Parameters like Solar Ultraviolet Radiation on the Survival of Microorganisms Petra Rettberg Bacterial Paleontology A.Yu. Rozanov

126 132

Paleobiological and Biogeochemical Vestiges of Early Terrestrial Biota: Baseline for Evaluation of Extraterrestrial Evidence Manfred Schidlowski

146

Formation of Ordered Structures of Charged Grains in Gas-Dusty Atmospheres of Planets and Comets during Lightning Discharge Yuriy G. Serozhkin

170

Exobiology of Titan Michael B. Simakov

175

The Role of Living and Nonliving Organic Matter in Volkonskoite Formation Y.S. Simakova

181

Astrobiotechnology: Alternative Concepts for Astrobiology Solar System Exploration Jan Toporski and Andrew Steele

187

The Study of Remains of Microorganisms in Ancient Earth Sedimentary Rocks for Astrobiology Galina T. Ushatinskaya, Elena A. Zhegallo and Emil L. Shkolnik

196

Recent Microbiology and Precambrian Paleontology Georgy A. Zavarzin

201

Author Index

217

Perspectives in Astrobiology R.B. Hoover et al. (Eds.) IOS Press, 2005 © 2005 IOS Press. All rights reserved.

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Nature of Framboidal Structures in Black Shales (the Cambrian of the Siberian Platform and the Permian of the Barents Sea Shelf) Marina M. ASTAFIEVA Paleontological Institute RAS 117997, Profsoyuznaya St., 123, Moscow, Russia Abstract. The origin of framboidal structures and their mineralogical composition (on the example of black shales of the Upper Permian of the Barents Sea Shelf and the Cambrian of the Siberian Platform) are discussed. The biogenic origin of framboids is confirmed.

Framboidal structures are common in Earth rocks and meteorites—carbonaceous chondrites. There is little doubt that the origin of framboids in astromaterial is the same as in Earth rocks. But up to now, there is still not a common opinion concerning the origin of framboids, i.e.: whether they are biogenic or not, so it is very important to solve the problem of the nature of framboids in Earth rocks. Framboids are spherical aggregates of microcrystals. They are characterized by a complicated, honeycomb inner structure and an inner portion of globules, which is monograined with a diameter of 0.1–10.0 μm. Some framboids are only partially mineralized by pyrite (FeS2). The close spatial connection between framboidal pyrite and the detritus of buried organic matter can be seen. Hence, the origin of framboidal pyrite is connected with mineralization of organic matter [1]. Framboids are found in a wide variety of sedimentary rocks of differing ages, and they are also found in recent swamp sediments, peat, marine, and oceanic silt. The origin of framboids by recrystalization of amorphous iron (Fe) sulfides in the early stages of diagenesis in the local niches of hydrogen sulfide is not excluded. The formation of framboidal pyrite is believed to be a result of the activity of sulfatereducing bacteria (SRB) [2]. Although the feasibility of abiotic precipitation of ironsulfides is well documented, the importance of bacteria in the sulfide precipitation process, at least in marine settings, is not in serious doubt [3]; however, there is no reason to exclude the possibility of an abiogenic origin of framboids because nearly all compounds, generally considered to be biological, are readily synthesized from abiogenic components in natural environments. Even protein amino acids have been shown to be assembled from abiogenic components during the crystallization and thermal ordering of hydrocarbons [4]. The role of bacteria in sulfide precipitation is great because the precipitation of iron sulfides requires high H2S concentrations, and in marine sediments, the rapid increase of H2S with depth is the direct result of sulfate reduction by bacteria. Although the precipitation is probably rarely biologically controlled, it is unquestionably biologically induced [3].

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M.M. Astafieva / Nature of Framboidal Structures in Black Shales

Figure 1. Framboids from: (a) and (b) the Upper Permian of the Barents Sea shelf (containing sulfur) and (c) (containing sulfur) and (d) (without sulfur) the Ogonyorian formation.

The black carbonate shales of the Kuonamka and Ogonyor formations of the Cambrian of the Siberian platform were chosen as objects of investigation. The sequences of both formations are situated in the Yudoma-Olenek region. Both formations are represented by the alteration of mudstones, siltstones and limestones, carbonate and siliceous rocks, and sapropelian. The age of formation is from Lower to Middle Cambrian [5]. In addition, the samples from the wells drilled on the Barents Sea Shelf near Mingasprom, Russia were studied. These rocks are the Upper Permian black, bituminous, and probably Posidonian shales. All samples were studied using CamScan. The chemical analyses were made using microzond analysis. All samples were treated by H2O2 for 30 min and heated in a muphel stove to exclude recent bacterial contamination. The microbial remains are mainly represented by framboidal structures. Framboids are numerous, and their diameters range from 3 to 10 μm (Fig. 1(a)–(d)). As a rule, framboids that are found are indivisible from (united with) the rock matrix, i.e.: they are indigenous to the rock. Rather often, it seems that the rock simply consists of these framboids, including the different layers (Fig. 1(a) and (b)). That is why there is no doubt that framboids are in situ, i.e.: they were formed simultaneously with the rock. Nevertheless, it is necessary to say that these framboids seriously differ in their chemical composition. Most of the framboids consist of sulfur (S) and iron (Figs 1(a)–(c) and 2) probably represented by pyrite. Framboidal pyrite is considered to be formed due to the activity of SRB [2]. The activity of these bacteria is connected with anaerobic conditions that are provided in the absence of oxygen. However, on account of the presence of SRB, it seems to be impossible to estimate the depth of paleobasin. Even the upper layer of a cyanobacterial mat a few millimeters thick provides anaerobic conditions beneath that are favorable for SRB development. The reception of sulfate from outside is the limiting factor for the development of such communities. The regeneration of sulfate is primarily possible by the oxidation of hydrogen sulfide under aerobic conditions and secondarily by the oxidation of H2S to sulfate under anaerobic conditions. As a whole, sulfidogenic assemblages play a great role in

M.M. Astafieva / Nature of Framboidal Structures in Black Shales

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Figure 2. Chemical composition of framboids.

marine conditions, and most organic matter in the bottom sediments is decomposed in such a manner [6]. It is necessary to mention that among framboids of iron sulfide there are framboids that are morphologically indistinguishable from pyrite framboids but lack sulfur in their chemical composition (Figs 1(d) and 2). Framboidal structures can sometimes be composed by magnetite. Bacterial magnetite can be formed in two ways: (1) By means of biologically induced mineralization and (2) by means of biologically controlled mineralization. In the case of biologically induced mineralization, organisms do not control the processes of biomineralization, and the mineral parts are formed extracellular. Magnetite is formed as a result of the activity of thermophilic and moderately thermophilic ironreducing bacteria under anaerobic conditions. Environmental parameters, such as Eh and pH, greatly influence the formation of magnetite. In this case, magnetite is a final product of vital activities of these bacteria. In the case of biologically controlled mineralization, minerals are deposited on or inside the organic matrix or inside of vacuoles in the cell. The organism controls, to some extent, the process of mineralization. Because the intracellular level of pH and Eh is defined by the organisms themselves, the formation of minerals depends on the environmental parameters to a lesser extent. In this case, the magnetic particles of magnetite are formed by magnetotactic bacteria. The magnetite structures that are analogous to framboidal structures are formed by multiple twinning, which is connected with the bacterial growth but not with the phase transitions or outside influences that are usually responsible for the twinning [7,8]. It is necessary to note that magnetite can potentially be a physical indicator of biologic activity. Iron framboids devoid of sulfur are not only represented by magnetite. It is known that a lot of iron sulfides, such as pyrite, macinawite (FeS1–x), and amorphous FeS, are metastable in typical oxidizing earth conditions and that is why they are rarely encountered outside microbial anaerobic conditions [9]. As far as nice hematite pseudomorphs of pyrite are known [10], it is possible to suppose that hematite could form pseudomorphs of framboidal pyrite as a result of oxidation. But in the studied samples, classic pyrite framboids were found simultaneously with framboids in chemical compositions from which S was absent. Therefore, it is possible to speak about the local formation of hematite.

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M.M. Astafieva / Nature of Framboidal Structures in Black Shales

The process of pyrite oxidation can probably occur with the filtration of surface waters through the rock containing pyrite framboids but not in underwater conditions because in that case the oxidation would touch the layer as a whole. The inclination is to favor the magnetite nature of framboids deprived of sulfur. The fact that pyrite and magnetite framboids could be found together can be explained by a certain deficit of a sulfate-ion in the basin of sedimentation. Moreover, both pyrite and magnetite are usually formed in warm water basins. In addition, the combined vital activity of SRB and iron-reducing bacteria should not be excluded. It is noteworthy that there is fossil benthic fauna in the studied intervals of sequences, i.e.: trilobites and brachiopods in Cambrian intervals and bivalves in the Upper Permian. However, the rock fragments with the benthic remains, in almost every case, are practically deprived of bacterial microstructures. In the bacteriomorph-enriched-microstructure fragments, there are no benthic macrofauna remains. This could probably be evidence of an irregularity of microbial transformation of organic matter and could be an indirect confirmation of the biological (bacterial) nature of our microstructures. There is an exception. The exception is the findings of remains of bivalve Posidonia in the Upper Permian black shales of the Barents Sea Shelf. Posidonia are a very peculiar, extremely thin-walled, flat bivalve. These fragile valves are noted in many samples; moreover, it seems that the best preserved pyrite framboids of are found in intervals with Posidonia. Posidonia characterize a particular facies in the Late Paleozoic and Early Mesozoic facies—usually occurring in bituminous, muddy sediments with plant debris, fish remains, and cephalopods. Benthic forms, such as brachiopods, corals, and bryozoans, are generally absent in the Posidonia facies. A lot of Posidonia, fishes, belemnite rostra, and hooks remains are the usual association of typical Posidonia shales. The lightness of Posidonia shells and the usual association of the genus suggest a pseudoplanatonic mode of life— perhaps these forms were attached by byssus to floating plants. The extreme thinness of the Posidonia shell valves also favors this assumption. Moreover, species of Posidonia are, as a rule, usually limited to dark shales containing such forms as fish and cephalopods during the entire history of their development [11]. That dark color of such sediments is considered to be caused by bituminous material, probably preserved under reducing conditions. Posidonia shale sedimentation probably occurred in a basin with stagnant waters, low maintenance of oxygen, and high maintenance of hydrogen sulfide. This corresponds to the data obtained by the analysis of the microbial remains of these deposits.

Conclusions The mineral composition of framboids is variable. Iron sulfides, especially pyrite, are predominant, and framboids of magnetite and perhaps of hematite are rather rare. The formation of framboidal structures is connected with the bacterial transformation and subsequent mineralization of organic matter. Framboids are deposited due to the vital activity of bacteria. There are two ways of framboidal formation, i.e.: biologically induced and biologically controlled mineralization; therefore, it is possible to speak about their biogenic origin.

Acknowledgements The author is grateful to everyone who has aided in conducting this work, especially A.Yu. Rozanov, E.A. Zhegallo, G.T. Ushatinskaja, V.I. Ustritskiy, T.M. Pchelina, N.V. Ustinov, and E.N. Preobrazhenskaya for their contribution in the discussion of the results and

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providing the rock material. The Author is also grateful to L.T.Protasevich for his assistance in electron microscope investigation. This study was supported by the Russian Foundation for Basic Research (projects 00–15–97764, 99–04–48806, and 00–05–64603).

References [1] Bogush IA, Burtsev AA. Ontogenesis of framboidal pyrite. In: Gavrilenko VV, Panina LK, Panova EG, Pinevich AA, Sukkarzhevsky SM, Vlasov DY, editors. Abstracts of the first international symposium, bio-inert interactions: life and rocks. St. Petersburg: St. Petersburg State University; 2002. p. 49–51. [2] Gerasimenko LM, Zavarzin GA. The relict cyanobacterial communities. In: The problems of preanthropogenous evolution of the biosphere, Moscow: Nauka; 1993. p. 222–53. [3] Kohn MJ, Riciputi LR, Orange DL. Sulfur isotopevariability in biogenic piryte: reflections of heterogeneous bacterial colonization? Am. Mineralogist 1998; 83(11–2) 2: 1454–68. [4] Yushkin NP. Biomineral homologies and organismobiosis. In: Mineralogy and life: biomineral homologies. Syktyvkar: Geoprint; 2000. p. 9–12. [5] Rozanov AYu, Repina LN, Apollonov MK, et al. Cambrian of Siberia. Novosibirsk: All-Russian Inc. Nauka, Siberian publishing firm; 1992. p. 135. [6] Zavarzin GA, Kolotilova NN. Introduction into environmental microbiology. Moscow: Knizhniy dom Universitet; 2001. p. 256. [7] Devouagard B, Posfai M, Hua X, Bazylinski DA, Frankel RB, Busek PR. Magnetite from magnetotactic bacteria: size distributions and twinning. Am. Mineralogist 1998; 83(11–2) 2: 1387–98. [8] Zhang Ch, Vali H, Romanek ChH, Phelps TJ, Liu ShV. Formation of single-domain magnetite by a thermophilic bacterium. Am. Mineralogist 1998; 83(11–2) 2: 1409–18. [9] Boston PJ, Spilde MN, Northup DE, Melim LA, Soroka DS, Kleina LG, Lavoie KH, Hose LD, Mallory LM, Dahm CN, Crossey LJ, Schelble RT. Cave biosignature suites: microbes, minerals, and Mars. Astrobiology 2001; 1: 25–55. [10] Godovikov AA. Mineralogy. Moscow: Nedra; 1975. p. 520. [11] Newell ND. Permian pelecypods of East Greenland. Medd. Gronland 1955; 110(4): 36.

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Bacteriomorphic Structures from the Sinsk Formation (Lower Cambrian of the Siberian Platform) Marina M. ASTAFIEVA Paleontological Institute RAS 117997, Profsoyuznaya St., 123, Moscow, Russia Abstract. The main types of biomorphic microstructures from black carbonate shales of the Sinsk formation (Lower Cambrian) of the Siberian platform are described. The possibility of the thin-layered part of the Sinsk formation being the vitally buried remains of cyanobacterial mat is discussed.

Introduction Some biomorphic structures of meteorites are practically indistinguishable from biomorphic structures of such Earth objects as black shales of the Sinsk formation of the Siberian Platform. That is why the black carbonate shales from the Sinsk formation were chosen as an object of investigation of fossil bacterial remains. Stratigraphically the Sinsk formation belongs to the middle part of the Botomian stage of the Cambrian and consists of the alteration of bituminous limestones and argillosiliceously-carbonate bituminous shales [1,2]. Rock samples from the type section of the Sinsk formation situated near the Sinyaya River (left tributary of the Lena River), and also from the Sinsk deposits from the region of Chekurovka (lower stream of the Lena River) were chosen for investigation, and the results of studies conducted by A. Yu. Rozanov and R. Hoover were applied. The preservation of biomorphs is different; rather often squashed and deformed, biomorphs smoothly pass into the rock and fuse with it. Sometimes it seems that the rock is composed from cocci and squashed tubes (Fig. 1(a) and (b)). Moreover, data of chemical analyses of rock matrix and biomorphic microstructures are identical; hence, it is possible to consider the bacterial remains to be found in situ. To exclude recent bacterial contamination, the samples were immersed in hydrogen peroxide for one-half hour and were dried in a muphel stove. The samples were studied under a CamScan 4 with a microanalyzer. The biomorphic microstructures in the rocks studied are represented by tubes, cocci, pyrite framboids, and thin threads, the formation of which are connected with activity of sulfate-reducing bacteria (SRB).

1. Tubes Single, long, empty tubes usually without branches are the most widely represented (Fig. 1(c)–(f)). The tubes form bundles occasionally, but there was no opportunity in this

M.M. Astafieva / Bacteriomorphic Structures from the Sinsk Formation

7

Figure 1. Biomorphic microstructures of Sinsk formation.

investigation to observe the sheaths of these bundles. There are traces of filament division into cells. The external surface of the tubes is often encrusted by relief papillae. There are two types of papillae. The first type of papillae is rounded or oval, sometimes weakly angular, very convex protuberances on the external side of the tubes (Fig. 1(c)–(e)). The surface of tubes with the second type of papillae resemble the texture of crocodile skin; the shape of these tubes in section is hill like (Fig. 1(f)). It seems that these papillae hills were formed by the curve of the tube wall and not by the thickness of it. Sometimes the tubes have a smooth surface. This is possibly connected with the peculiarities of mineralization or with the subsequent destruction or recession of these papillae.

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Regarding the biological nature of such papillae, it could be proposed that papillae are the biomorphic microstructures attributed to cyanobacteria; the tubes covered by papillae to some extent look like the picture of phage-defeated filamentous bacteria [3] and to a lesser extent resemble parasitizing vibrion found on chlorella cells [4]. In the chemical composition of the tubes and surrounding rocks, calcium (Ca) and silicon (Si) predominate; therefore, it is possible to propose silification or carbonatization of cyanobacterial cover. Moreover, tubes with papillae are practically indistinguishable from Phormidium—cyanobacteria, which are typical for thermophilic mats—encrusted by small siliceous beads, found in the discharge apron of thermal springs in New Zealand [5]. However, it is too early to make final conclusions because the rocks by themselves are argillaecarbonate, i.e.: they are comprised of both calcium and silicon. Among the studied biomorphic structures, tubes with papillae predominate. Judging by morphology, size, character of connection of tubes, and their division into cells of corresponding size, tubes with papillae are considered to be cyanobacteria, which play the leading role in cyanobacterial mats—specific stable bacterial communities. Cyanobacteria are the basis of such communities. In this case, the main synthesis of organic matter proceeds because of photosynthesis realized by cyanobacteria in the aerobic zone. In all recent mats, oscillatorial forms predominate as active filament forms. Under extreme conditions for the development of cyanobacteria, anoxygenic photosynthesis is provided by both green and purple photothrophic bacteria.

2. Cocci In addition to tubes, spherical forms known as cocci are widely distributed in our samples (Fig. 1(g)). They exist both as single forms set in the rock and as accumulations or colonies. Cocci often surround tubes and are sometimes the main element of the rock. Judging from positions of morphology, the signs of these cocci correspond to signs of purple bacteria.

3. Pyrite Pyrite is spread in different layers of rocks under investigation. The pyrite exists both in framboid shape that is typical for thermophile cyanobacterial mats [6]. The presence of pyrite automatically suggests the process of sulfate reduction that is produced by SRB. These bacteria use elemental sulfur and sulfates, which are formed as a result of photosynthesis, and trophically SRB are closely connected with the purple sulfur bacteria. In the presence of sulfates, SRB produce H2S that in turn can be used by purple sulfur bacteria in the process of anoxigenic photosynthesis. As a result, the sulfate is produced and can be used by SRB in its own turn. The development of sulfidogenics—SRB—is typical for the lower anaerobic zone of the cyanobacterial mat [4,7]. In silts or in dark anaerobic zones, the H2S is connected in dissoluble iron sulfides, falls into deposits, and exits the sulfur circle. With sufficient illuminaton, the phototrophic purple bacteria are the main consumers of sulfuretted hydrogen. In the case of a deficit of sulfuretted hydrogen, the sulfates are the main products of H2S oxidation, and in this case the sulfur is not accumulated. If the rate of formation of H2S or the rate of its admission is more than the rate of its oxidation by microorganisms, sulfur is formed immediately inside the cells of purple sulfur bacteria [3]. In the investigated specimens, pyrite us very rarely found, but cocci of purple bacteria are rather abundant. The data of chemical analyses deny the presence of sulfur in the studied samples. Consequently there was probably no H2S deficit. That is why it is reasonable

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to suggest that the formation of Sinsk rocks occurred in a photic zone. The pyrite formation was connected with the daily fluctuations of illumination. The deposition of the iron sulfide proceeded only while it was dark when the use of H2S by the purple bacteria was stopped. When it was light, the H2S was used by the purple bacteria. These findings support the theory that the microorganisms found formed cyanobacterial mats during Sinsk time. These mats are the benthic communities of microorganisms in which phototrophic bacteria are dominant. Among them, cyanobacteria are the main producers of organic matter and are responsible for the structure of the mat. Since recent cyanobacterial mats are represented by benthic forms, it is suggested that a benthic mode of life of the bacteria from the Sinsk formation form cyanobacterial mats. Therefore, it is possible to say that the Sinsk basin was relatively shallow watered, i.e.: the depth of basin should correspond to the photic zone. The fossil bacteria in the Sinsk deposits were found to be the most abundant and diverse in thin-layered parts of the sequence and a little less diverse in the more solid parts of the sequence. It is well known that all cyanobacterial communities form expressive layered structures with the characteristic alteration of mineral layers with development zones of different microorganism groups. Since the mats are only slightly pervious, the formation of minerals in thin layers connected with the type of bacteria is assisted. It cannot be excluded that it is the layered structure of the cyanobacterial community that is responsible for the presence of tubes with papillae—cyanobacteria—in thin-layered rocks. Sometimes it looks as if these rocks consist of bacterial remains. The fact that the communities were buried in vital position is an advantage. The preservation of the layered structure serves as a confirmation of such a conclusion. Hence, it can be suggested that the thin-layered part of Sinsk formation is mainly vitally buried remains of cyanobacterial mat. The presence of cyanobacteria by themselves in the Sinsk formation suggests the formation of its rocks in the photic zone, i.e.: under conditions of a relatively shallow-water basin and correspondingly about sufficient shallow waters of the Sinsk basin as a whole [8]. 4. Thin Threads There is one other type of filamentous biomorphic structure in specimens under investigation. This type is represented by very thin, straight threads or threads with branches (Fig. 1 (e)–(f)). In the recent stage of investigation these threads are considered to be actinomycetes. But these forms appear to be embedded in surface; hence, these forms can be considered to be later contamination. Acknowledgments The author is grateful to everyone who has promoted this work, especially A.Yu. Rozanov, E.A.Z Zhegallo, G.T. Ushatinskaja, and L.M. Gerasimenko for their contribution to discussion of the results, and L.T. Protasevich for his assistance in electron microscope investigation. This study was supported by the Russian Foundation for Basic Research (projects 00–15–97764, 99–04–48806, and 00–05–64603). References [1] Lower Cambrian stage subdivision. Stratigraphy 1984; 184. [2] Rozanov AYu, Repina LN, Apollonov MK, et al., Cambrian of Siberia. Novosibirsk. All-Russian Inc. Moscow: Nauka;1992. p.135.

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[3] Gorlenko VM, Dubinina GA, Kuznezov CI. Ecology of water microorganisms. Moscow, Nauka. [4] Gromov BV, Pavlenko GV. Ecology of bacteria. L.:University Press; 1989. p. 248. [5] Jones B, Renaut RW, Rosen MR. Microbial biofacies in hot-spring sinters: a model based on Ohaaki Pool, North Island, New Zealand. J. of Sedimentary Res., 68:1998; 413–34. [6] Zavarzin GA, The development of microbial communities in the history of Earth. The problems of preanthropogenous evolution of the biosphere. Moscow: Nauka; 1993. p. 212–21. [7] Gerasimenko LM, Zavarzin GA. The relict cyanobacterial communities. The problems of preanthropogenous evolution of the biosphere. Moscow: Nauka; 1993. p. 222–53. [8] Rozanov A Yu, Zavarzin GA. Bacterial paleontology. Herald of the Russian Academy of Sciences 1997:67; 109–13.

Perspectives in Astrobiology R.B. Hoover et al. (Eds.) IOS Press, 2005 © 2005 IOS Press. All rights reserved.

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Constraining Subglacial Settings Using Clay-Supported Ice Rafted Detritus (Mud Grains) in Antarctic Marine Sediment: A Framework for Astrobiology Rosalba BONACCORSIa,*, Antonio BRAMBATIa, Lloyd H. BURCKLEb and Alexander M. PIOTROWSKIb a Dip. di Scienze Geologiche, Ambientali e Marine (DiSGAM) University of Trieste, Via E. Weiss, 2 34127, TS, Italy b Lamont-Doherty Earth Observatory, Columbia University, Rt. 9W Palisades, NY 10964, United States * Geokarst Engineering s.r.l AREA Science Park, Padriciano 99-34012, TS, Italy (present address) Abstract. The subglacial Antarctic Ice Sheet is one of the lesser known and most inaccessible places for direct sampling. This work, conducted under the Italian Program for Antarctic Research (PNRA), aims to use results of multicomponent analyses and observations on ice proximal marine sediment cores (Ross Sea, Glomar Challenger Area) as the key data set to introduce the first general sedimentary model(s) into an Astrobiology Roadmap scientific scheme, i.e.: Goals 5 and 8. Information obtained from Antarctic glacigenic sediments can provide plausible models for planetary bodies where glacial ice fields and related processes occur (i.e., the ice caps of Mars, and Jupiter’s icy moon, Europa). The analyses (Corg and biogenic opal) on diamicton mud grains (MDGS) suggest that fine-grained ice rafted detritus (IRD) can retain their original depositional settings, e.g.; exposed outcrops and subglacial lake basins, after incorporation within marine sediment and provide some information on the Antarctic interiors eroded by the East and West Antarctic Ice Sheets. Finally, observations on marine and ice cores suggest that MDGS and siltclay aggregates are more widely distributed throughout Antarctic sediments and glacial fields than previously believed. The most reliable models should consider potential sources and processes/mechanisms explaining high-Corg content in subglacially-derived material. Ice proximal marine sediment would provide an unlimited amount of MDGS samples as continent-derived material as test sources of organics of use in astrobiological research.

Introduction Among a variety of extreme settings, e.g.: permafrost, ultra-cold deserts, ice covered lakes, and subglacial cavities, the subglacial Antarctic Ice Sheets are among the lesser known and most inaccessible places to sample and approach through remote observations. Goals 5, 7, and 8 of the science scheme of the NASA Astrobiology Roadmap [1] address constraints on the limits of life in past- and present-day extreme environments. Information obtained from fine-grained IRD can provide plausible models for Antarctic glacial ice fields and subgla-

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Figure 1. Antarctic map showing the study area and sites with MDGS-associated observations—marine (solid dots), sea-ice cores (diamonds), and areas where subglacial lakes have been remotely detected (triangles) [14,15]: (1) Byrd Ice Core [16], (2) Vostok Ice Core [17,18], (3) Dry Valleys, and Taylor Glacierassociated moraines deposits [19], (4) sea-ice core at J–9 site [20], (5) J–9 site—sub-ice shelf sediments [7], (6) tertiary diamictons from CRP–1 [12], (7a) and (7b) late Quaternary marine sequences from the Western Ross Sea [8,13], (8) Prydz Bay [8], (9) cores ANTA95–77C2 [4] and ANTA95–89C outer slope settings (dots), (10) core ANTA98–16 (star) (M. Romana, personal communication, 2001); and (11) other central Eastern Ross Sea cores [21].

cial pools. Those extreme settings represent useful test beds for Mars ice caps [2] and icy moons, such as Europa, where analogue environments have been observed and/or are expected [2,3]. Glaciomarine diamicton sequences from the Antarctic continental margins (ice proximal zone) are mostly made up of in situ marine sediment mixed with variable amounts of subglacially derived material, i.e.: IRD including MDGS (Figs 2(b) and 3(b)–(d)) [4,5]. All IRD, and thus, diamicton MDGS, are definitely glacially scoured from the Antarctic interiors by the West Antarctic Ice Sheet (WAIS) (Fig. 1) and East Antarctic Ice Sheet (EAIS). As a result, cores from the ice proximal zone (Figs 1 and 2(a)) can also recover material from large areas associated with their (palaeo) drainage basin [6–11]. Downcore abundance and the composition of IRD lithic fractions in these types of sediment (Fig. 3) are generally used as proxies for change in the palaeoclimate-palaeoenvironmental signal, e.g.: calving events resulting from glacial/interglacial pulses of the ice sheet/ice shelf system, or for tracking sediment provenance [4–5,7–13]. Here the IRD are observed using a different paradigm. Why Are Antarctic Diamictons Relevant to Astrobiology-Addressed Research? Here we will support evidence that clay-supported IRD MDGS incorporated in Antarctic marine sediment, and/or diamicton matrix, can still retain information concerning their original settings. Although many possible sources can be expected for MDGS, this work mainly deals with possible provenance from subglacial sources, which are widespread beneath the EAIS, e.g.: subglacial lake basins in the East Antarctic Craton [14,15], and WAIS, e.g.: Byrd Basin area [6]. Then, results of multi-component analyses and observa-

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Figure 2. (a) Schematic sketch of the Antarctic continental shelf and slope with bathymetric depth and core locations, and (b) example of glaciomarine sediment containing iceberg rafted debris (IBRD) and MDGS from the deep-sea core ANTA95–89C.

Figure 3. (a) Chronostratigraphy of Core ANTA95–77C2 with indication of sampled depth-intervals and (b)– (e) photographs of MDGS/Matrix samples.

tions on ice proximal marine sediment cores (Ross Sea and Glomar Challenger Area) are used to draft the first general sedimentary model(s) of the Antarctic ice cap subglacialcontinental margin system into an Astrobiology Roadmap scientific scheme [1]. Building a conceptual model for the exchange of fine-grained debris and thus of energy between the atmosphere and the Antarctic subglacial habitats and between the Antarctic subglacial habitats and the sea would provide a useful test bed for two relevant astrobiology-related issues.

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First, the study of terrestrial analogues, such as subglacial diamicton and ice proximal glacial marine sediment, can aid prediction for similar settings at the Mars polar regions [2]. Thus, if continental/subglacial sources of organic matter can be unequivocally retained and unraveled in glacial marine sediment, the same type of information could be obtained from those Mars polar regions where they are expected. In fact, in Mars’ polar environment, IRDs and fine-grained sublimation tills (requiring cold and arid extreme) are considered suitable terrestrial analogues of Martian floods and their sampling was proposed under the Mars Pathfinder (MPF) landing-site selection [2]. Second, such a model would frame the possibility that subglacial lakes are really the most isolated ecosystem on Earth. Indeed, it is thought that subglacial lakes, such as Lake Vostok, are valuable analogues for possible ice-covered oceans of icy moons, such as Europa and Callisto [3].

1. Background 1.1. Mud Grains Are Widely Distributed in Glaciated Areas MDGS were first recognized as nonlithic, mud-supported ice-rafted particles in core ANTA95–77C2 (75° 50.0' S and 177° 42.9' W; at 627-m depth and 118.5-cm long) [4] and core ANTA95–89C (74° 29.100' S and 175° 34.059' W at 2058-m depth and 404-cm long (outer Slope) (Figs 2(a) and (b) and 3). Mud-supported particles were observed in a variety of cases. The map of Antarctica (Fig. 1) shows sites with MDGS-associated observations.

2. Material and Methods Multiple analyses of selected mud grains, sedimentary rock particles (SRP), and their hosting matrix were conducted on large-sized samples (30–50 mg). They were extracted from Unit A (glacial marine to open-sea lithofacies), Unit B (reworked diamicton), and Unit C (subglacial diamicton) of Core ANTA95–77C2 (Fig. 3) [4,5]. Selected grains were gently removed from external layer in order to ensure a few - mg aliquots of pure sample for separate analyses. The supporting matrix was crushed into small fragments for obtaining representative MDGS-free samples. A PerkinElmer® 2400 CHN Elemental Analyzer and a Carlo Erba® NA1500 were used for elemental analysis of total carbon and total organic carbon (TOC) determination. CaCO3 was measured with a carbon dioxide coulometer. Stereoscope, microscope, and smear slide observations (with a petrology microscope) were made to identify mud grain types and evaluate their qualitative content (fine-grained biogenic and mineral particles). Scanning electron microscope (SEM) photomicrographs on silty-sized centrifuged material were taken with a Leica® Stereoscan 430i. Full details have been provided [10,14,22].

3. Results MDGS contain higher TOC (0.36–0.77%; 0.57±0.09%; n=16) than the supporting matrix (0.29–0.51%; 0.40±0.06%; n=15) and SRP (0.16–0.43%; 0.32±0.09%; n=10) (Fig. 4 (c)). In MDGS, CaCO3 is the most variable parameter (0.09–54.4%; 0.32±0.09%) (Fig. 4 (a)); biogenic opal is constant throughout the matrix (12.91±16.43%; 15.1±1.1%; n=8) (Fig. 4(b)

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Figure 4. XY diagrams showing: (a) TOC versus Opal, (b) CaCO3 versus Opal, (c) TOC versus CaCO3, and (d) TOC matrix versus TOC component. See Section 4 for explanation.

and (d)) but highly variable in MDGS (4.2–44.0%; 32.8±14.4%; n=7). Matrix and MDGS belong to separate fields of the XY diagrams (Fig. 4 (a)–(d)) and show statistically significant compositional (z-Test two sample for means, two-tails: p<0.01) and textural differences. The ample range of Corg content (0.05–54.4%) found in MDGS, thus, could indicate quite different sedimentary settings. Furthermore, Sample GS–Y, 95–97 cm, contains small numbers of late Pleistocene diatoms (Opal=2.7%wt, clay-sized fraction) while authigenic minerals, i.e.: gypsum, carbonates, occur in the silt-sized fraction (SEM observation). In this sample, the extremely high Corg (TOC=~4.8%) and authigenic calcite (CaCO3=54.4%) highly contrast with values found in the embedding matrix, i.e.: Sample MX–95–97 cm (TOC=0.43%; CaCO3=0.21%; and Opal=~14%), and occur together with a mantle-derived radiogenic isotope signature, i.e., epsilon Nd(0)=~+4.6 and 87Sr/86Sr = 0.704–0.705 (for the leached, i.e.: carbonate-free, fraction) [10]. Those values resulted within the range of Antarctic Ice core Dome C [22], are associated with volcanic-derived detritus. This might indicate a subglacial setting where both volcanic debris (either from dust particles, or subglacial mud volcanoes sources) and relatively abundant organic sources are available. The highest TOC content of Sample GS– Y, 95–97 cm could derive from either organic-rich sources or efficient mechanisms of concentration of organics.

4. Discussion Several types of MDGS were observed (Fig. 3 (b)–(e)). First, the geochemical (Fig. 4) and textural variability [10,11] between the MDGS and the matrix indicate different sources and, at least for the studied cases, confirm a separate origin from their hosting matrix. Second, their widespread TOC, CaCO3, and opal % contents (Figs 4a–d) suggests that they can retain different sedimentary environments. The possibility that such grains can maintain the geochemical identity after their incorporation into over compacted and soft diamictons is in agreement with former observation of ice rafted material, i.e.: till pellets, incorporated in bottom marine sediment from their sources [18].

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Figure 5. SEM microphotographs of bulk silt-sized detritus from Sample GS–Y 95–97 cm.

At this point, a general model is needed; one that takes into account the widespread presence (geographic, environmental, and stratigraphic) and composition of such grains and draws relationship with their potential source areas (PSA).

5. Models, Sources, Processes, and Lithospheric Setting The most reliable models should consider the four following possibilities: (1) Potential sources, (2) processes at the ice sheet/bedrock interface, (3) alternative mechanisms explaining high degree of compaction of MDGS, e.g.: colloidal fractions bounding in ice pores [23], and (4) a final step consisting of embedding/preservation of MDGS within different settings, i.e.: subglacial, glacial marine, and open-sea sediment. 5.1. Potential Sources Subglacial pools throughout the East Antarctic Craton and West Antarctic Rift System are potential sources. Although TOC values alone are inadequate to distinguish among different sources of organic material, it is reasonable to hypothesize that certain amounts of organics found in MDGS could have some microbial source. Specifically, grains, such as Sample GS–Y, 95–97 cm (Fig. 3 (d) and Fig. 5) might have embedded fine-grained detritus from subglacial lake/pool systems. It is well known today that heterotrophic bacteria occurs in subglacial lake-associated sediments, such as those discovered near the basal layer of the Vostok ice core [24]. This type of bacterial material could be exported, then, toward more distal settings, e.g.: glaciomarine sediment, from glaciers overriding the lake basin and by silt-sized particles adhering to subglacial/englacial layers of freeze-on material. This possibility can be argued from the following: • • •

Muddy palletized material is currently observed from basal portions of ice cores, including the Vostok ice core. The widespread presence of subglacial lakes (up to 76 distinct basins) is well established through ice-penetrating radar from continental areas, such as the East Antarctic Craton [14,15,25] and the West Antarctic Rift. Those areas are part of a drainage system. This implies the existence of links between the subglacial pool systems and overriding ice sheets [15], and between the ice stream’s flow trajectories into the Ross Ice Shelf (RIS) and its outward continental margin [10].

In addition, the presence of authigenic calcium carbonate and gypsum, associated with abundant organic matter (Fig. 5), is in agreement with those observations made on the

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dirty-ice basal layer of the Vostok ice core (John Priscu, 2001 personal communication) containing subglacial microbial loop [17,18,24]. Furthermore, the presence of framboidal pyrite indicating low-energy/reducing environments could be consistent with such a source. At this point, it must be said that the estimated microbial biomass for Dry Valley Lakes, e.g.: Fryxell, Hoare, and Bonney, is several orders of magnitude higher (0.3–5 µg C L–1 and 436–818 µg C L–1) [26] than those found in the Vostok accreted ice (<0.1–0.003 µg C L–1) in which oligotrophic conditions, i.e.: TOC=6.6–7.5 µmol L-1) are expected [24]. However, the amount of organics in the near-surface sediments surrounding Lake Vostok may be higher than those found in the accreted ice if concentration mechanisms were acting there. Also, subglacial lakes other than Vostok could have different degrees of trophic conditions. Such a subglacial pool could have provided clay material to form certain types of MDGS. 5.2. Other Sources Sources other than subglacial lakes can be inferred from observations made on some mud grains. MDGS might be related to different modes of superglacial, subglacial to englacial drift at the bedrock/ice-sheet interface. For instance, ice-covered (epiglacial) lakes as those just mentioned above [26] could provide some organic-rich material. Furthermore, MDGS could represent the following four cases: (1) The remains of unconsolidated sedimentary deposits from land, e.g.: Beacon Supergroup, or exposed soils/permafrost from the ultra cold Dry Valley region near Taylor Glacier [19] and the Transantarctic Mountains; (2) stiff, but still remolded material, simply eroded from the exposed inner shelf by overriding grounded ice shelves during glacial advances or wind blown during major katabatic wind events; (3) the upstream erosion of subglacial marine-derived sedimentary basin located in the central Eastern Ross Sea [6,7,21]; and (4) marine sediments affected by sub marine erosion through gravitational processes. In case 3, sources of reworked/old carbon and varying amounts of biogenic opal could be beneath WAIS [20] and RIS where sedimentary basins of tertiary age occur. Furthermore, according to case 1, well-rounded quartz, i.e.: sand-sized grains, included in some MDGS may indicate that they were wrapped by some adhering organic-bearing clay, probably after erosion from sandstone in the Beacon group (south of David Glacier, East Antarctica), as reviewed by Anderson et al., (1992).

6. Models 6.1. Conceptual Model Figure 6 attempts a schematic, integrated model of WAIS, incorporating potential sources and processes, e.g.: freezing-on, responsible for the exchange of mineral and organic debris at the ice-sheet ice-sediment interfaces and throughout different Antarctic settings, i.e.: atmosphere, cryosphere, land, and sea. The interior ice reservoir below the ice divide is the portion of the ice sheet coupled with its bed. The ice slides over its bed from the onset region towards the ice shelf (open arrows). The fast-moving glaciers, i.e.: ice streams A–F, drain the interior ice flowing between regions of relatively stagnant ice (ice domes) and penetrate the RIS. The lubricating till lies beneath the ice streams and the graben system (or the East Antarctic Craton System), which is filled by sediments. Basal melting at the ice/sub-ice and gravitational transport would allow sinking of windblown materials (atmospheric sources) throughout the ice caps in an open rather than closed-system. Entrainment of material (rock flour and ancient marine sediment) from subglacial systems and links with atmosphere and coastal setting are also shown by different types of arrows.

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Figure 6. Schematic model of WAIS (modified from http://www.ig.utexas.edu/research/projects/wais).

7. Processes 7.1. Sediment Caption Caption/uploading, transport, and deposition of subglacial fine-grained sediments by glaciers and ice streams has to deal with those subglacial processes, i.e.: freeze-on, occurring at the sediment bed/ice interface [6,7,10,26]. In this framework different basal ice/thermal conditions (above and below the freezing point) have been proposed, e.g.; wet- to dry-based glaciers and ice sheets [26]. These conditions could be important because, among other things, they could either favor or contrast the formation/persistence of mud grains and processes responsible for the accretion of clay material around lithic nuclei, as well. 7.2. Incorporation in Different Types of Diamicton Matrix Some grains appeared to be more compositionally similar to their host diamicton matrix, e.g.: tertiary diatom-bearing grains. This may result from more interactions, e.g.: subglacial stress in over compacted diamicton, between grains and host matrix during their incorporation within the matrix itself and/or the deposition of glaciomarine diamictons. Indeed, several steps could be possible between the incorporation of fine grained sediment in the basal ice sheet and, thus, the world-wide presence of mud pellets in ice cores; their embedding into subglacial diamicton as ice shelf rafted debris; and the release of plastic mud grains after calving as IBRD (Fig. 2 (a)). The strong resistance to mixing of MDGS found in sedimentary sequence from ice shelf located cores only apparently contrasts with the instability on melting observed for those muddy particles that were tentatively isolated from Arctic and Antarctic ice cores [10].

8. Conclusions and Final Remarks 1. Unraveling the biogeochemical signals retained in subglacial ice rafted materials (Antarctic analogs) would provide a relevant issue for sampling return missions focused on Mars polar cap candidates where similar deposits are expected.

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2. Compositional and textural differences in mud grains must be the result of a combination of different glacial/subglacial sources and processes involving different types of materials (soils, loose sediment, and sedimentary sequences). 3. Marine sediment core samples, therefore, offer practical advantages—such as the ability to test a wide variety of subglacial settings deposited at different times, e.g.: Mesozoic to Pliocene and late Pleistocene to recent; an unlimited amount of different sources providing direct sampling on subglacial ecosystems from the past; and improved information to constrain subglacial models. 4. Improved conceptual model for the exchange of organic debris throughout different Antarctic compartments (atmosphere, cryosphere, land, and sea) would test the hypothesis that Antarctic subglacial lakes are a real isolated ecosystem and, thus, provide useful analogues for the ice-covered ocean(s) of Europa. 5. The extensive use of MDGS in astrobiological research should be tested using (1) elemental, chromatographic, and stable isotope analyses (EA-IRMS, and GC-MS) on bulk organics, e.g.: δ13C-org, δ15N-tot/org, and associated biomarker compounds (M. Romana, personal communication, 2001) and (2) a combination of advanced techniques, e.g.: Epifluorescence, FESEM, and ion microprobe, to search for microfossils, dormant spores, viable bacteria [19], and any associated biomarkers, e.g.: biologically-precipitated mineral phases.

Acknowledgments This work was funded by PNRA, the Office of Polar Programs (National Science Foundation) to lHB and a grant/cooperative agreement from the National Oceanic and Atmospheric Administration (NOAA). The authors are grateful to R.F. Anderson and S. Hemming for supporting TOC and Carbonate measurements and radiogenic isotope data at LamontDoherty Earth Observatory (L-DEO); and F. Drake (SETI Institute) for an early review of this work. Also, special thanks go to G.P. Fanzutti, F. Finocchiaro (DiSGAM), and R. Melis for valuable discussions. Special thanks are also due to L. Barker and P. Malone (L-DEO), and T. Quaia (for assistance with analyses at L-DEO and DiSGAM, respectively), and T. Ubaldini (University of Trieste) for assistance with SEM. The views expressed herein are those of the authors and do not necessarily reflect the views of NOAA or any of its sub-agencies.

References [1] Morrison D, Schmidt GK. NASA Astrobiology Roadmap. Moffet Field, CA: ARC 1999; 1–44. http://astrobiology.arc.nasa.gov/roadmap/goals/index.html. [2] Rice JW. Getting the first crack at Noachian clasts and sediments: a pathfinder’s prospectus. In: Workshop on Early Mars: Geologic and Hydrologic Evolution, Physical and Chemical Environments, and the Implications for Life. Houston, TX: April 24–27, 1997. http://www.lpi.usra.edu/meetings/earlymars/ pdf/3054.pdf. [3] Carr MH, Belton MJ, Chapman CR, Davies ME, Geissler P, et al. Evidence for a subsurface ocean on Europa. Nature 1998; 391: 363–5. [4] Bonaccorsi R, Brambati A, Finocchiaro F, Quaia T. From Basal till to Open-water sedimentation: late Quaternary to Early Holocene changes from Core ANTA95–77C2 (Glomar Challenger Basin, Ross Sea). Terra Antartica Report 2000; 4: 241–58. [5] Bonaccorsi R, Burckle HL, Brambati A, and 4 other authors. Multi-component analyses on Diamicton Mud Grains (Glomar Challenger, Ross Sea, Antarctica): can they track sources and processes related to the Ice Sheet/Ice Shelf System? Suppl. to EOS 2000; 81(19): 269. [6] Truswell EM, Drewry DJ. Distribution and provenance of recycled palynomorphs in surficial sediments of the Ross Sea, Antarctica. Marine Geology 1984; 59: 187–214.

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[7] Webb PN, Ronan TE, Lipps JH, DeLaca ??. Miocene Glaciomarine Sediments from beneath the Southern Ross Ice Shelf, Antarctica. Science 1979; 203: 435–7. [8] Domack EW, Harris PT, Taylor F, Quilty PG, De Santis L, Raker B. Late Quaternary sediment facies in Prydz Bay, East Antarctica and their relationship to glacial advance onto the continental shelf. Antarctic Science 1998; 10(3): 236–46. [9] Domack EW, Harris PT. A new depositional model for ice-shelves, based upon sediment core from the Ross Sea and the Mac Robertson shelf, Antarctica. Annals of Glaciology 1998; 27: 281–4. [10] Bonaccorsi R. Evolution of the Ice Sheet - Ice Shelf - Continental margin system (Ross Sea, Antarctica) from late Quaternary sedimentary records. University of Trieste 2001; Ph.D. thesis: 1–241. [11] Bonaccorsi R. Investigation on the non-lithic Ice rafted debris (Mud Grains) as source of continental/reworked organic matter affecting AMS 14C dating of Antarctic marine sediments. In: Young Researchers Project 2nd Year. University of Trieste 2002; Internal Report: 1–60. [12] Van der Meer JJM, Hiemstra JF. Micromorphology of Miocene Diamict, indication of grounded Ice. Terra Antarctica 1998; 5(3): 363–6. [13] Domack EW, Jacobson EA, Shipp S, Anderson JB. Late Pleistocene-Holocene retreat of the West Antarctic Ice Sheet system in the Ross Sea: Part 2 – Sedimentologic and stratigraphic signature. GSA Bulletin 1999; 111(10): 1517–36. [14] Siegert MJ, Dowdeswell JA, Gorman MR, McIntyre NF. An Inventory of Antarctic sub-glacial lakes. Antarctic Science 1996; 8: 281–6. [15] Siegert MJ, Kwok R, Mayer C, Hubbard B. Water exchange between the subglacial Lake Vostok and the overlying ice sheet. Nature 2000; 404: 643–6. [16] Gow AJ, Meese DA. Nature of basal debris in the GISP2 and Byrd ice cores and its relevance to bed processes. Annals of Glaciology 1996; 22: 134–40. [17] Jouzel J, Petit JR, Souchez R, et al. More than 200 meters of lake ice above subglacial Lake Vostok, Antarctica. Science 1999; 286: 2138–41. [18] Priscu ??, et al. Geomicrobiology of Subglacial Ice Above Lake Vostok, Antarctica. Science 1999; 286: 2141–4. [19] Fitzsimons SJ. Formation of thrust-block moraines at the margins of dry-based glaciers, south Victoria Land, Antarctica. Annals of Glaciology 1996; 22: 68–74. [20] Zotikov IA, Jacobs S. Oceanic inclusions in the J-9 sea-ice core. Antarctic Journal of the U.S. 1985; 20(5): 113–5. [21] Kluiving SJ, Bartek LR, van der Wateren FM. Multi-scale analyses of subglacial and glaciomarine deposits from the Ross Sea continental shelf, Antarctica. Annals of Glaciology 1999; 28: 90–6. [22] Grousset FE, Biscaye PE, Revel M, Petit JR, Pye K, Joussaume S, Jouzel J. Antarctic (Dome C) ice-core dust at 18 kyr. B.P: Isotopic constraints and origins. Earth and Planetary Science Letters 1992; 111: 175–82. [23] Ovenshine AT. Observations of Iceberg Rafting in Glacier Bay, Alaska, and the Identification of Ancient Ice-Rafted Deposits. GSA Bulletin 1970; 81: 891–4. [24] Karl DM, Bird DF, Björkman K, Houlihan T, Shackelford R, Tupas L. Microorganisms in the Accreted Ice of Lake Vostok. Science 1999; 286: 2144–7. [25] Kapitsa A, Ridley JK, Robin G, Siegert MJ, Zotikov I. Large deep fresh-water lake beneath the ice of central East Antarctica. Nature 1996; 381: 684–6. [26] Takacs CD, Priscu JC. Bacterioplankton Dynamics in the McMurdo Dry Valley Lakes, Antarctica: Production and Biomass Loss over Four Seasons. Microbial Ecology 1998; 36: 239–50.

Perspectives in Astrobiology R.B. Hoover et al. (Eds.) IOS Press, 2005 © 2005 IOS Press. All rights reserved.

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Apsidal Motion Problem in the Eclipsing Binary Star DR Vulpeculae Caner ÇIÇEK Çanakkale Onsekiz Mart University, Faculty Arts and Sciences, Department of physics, TR-17100 Çanakkale, Turkey [email protected] Abstract. Photoelectric observations of the DR Vulpeculae (Vul) have been carried out in B and V colors at the Ege University Observatory and new light curves have been obtained for the system. The O-C diagram was analyzed using all reliable timings found in the literature and new values for the elements of the apsidal motion was computed. The apsidal motion period of the system, 36.8 yr, was obtained.

Introduction The variability of DR Vul (BD+260 3835=HDE 339770) was discovered in 1935 by Hoffmeister, [1]. In 1950, Tsesevich [2] assigned DR Vul to the β Lyr type and determined its period. Erloksova [3] constructed a mean light curve for DR Vul. The form of the mean light curve enabled Erloksova to assign this system to the Algol-type eclipsing stars. In investigating the variation of the period of DR Vul, Erloksova discovered a rotation of the line of apsides with a period 25 yr. Semeniuk [4] obtained the first photoelectric measurements of the brightness of DR Vul. Semeniuk constructed an O-C graph and from it, estimated the period of rotation of the line of apsides, U=38.5 yr, e=0.092, w=25.4 for the epoch of 1950. O’Connell [5] constructed the first complete photoelectric light curve of DR Vul and determined the photometric elements of the system. The O-C graph, based on photoelectric times of minima alone, enabled the determination the period of apsidal rotation, U=37.8 yr. Khaliullina [6] found a value of 36 yr and suggested the possibility of a superposition of two additional longer periods due to light-time effects. The light curve was published by Khaliullina and Khaliullin [7]. The apsidal motion of DR Vul was discussed by Wolf and Diethelm [8]. Finally, Wolf et al. [9] found a value of 36.3 yr for apsidal motion.

1. Observations DR Vul was observed photoelectrically at the Ege University Observatory on 40 nights during The 1993 and 1994 observing seasons. All observations were made with B and V filters which are very close to Johnson’s standard system. BD 260 3827 and BD 260 3837 were used as comparison and check stars, respectively. The data related to the variable comparison and check stars are given in Table 1. During the observations, no significant light variation of the comparison and check star was found. The atmospheric extinction coefficients in each color for each observational night were calculated from the observations of the comparison star using conventional methods. Then, all the instrumental differential B and V

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Table 1. The data for the observed stars.

Figure 1. The light and color curves of DR Vul in 1993.

magnitudes (in the sense of variable minus comparison) were corrected for atmospheric extinction and the light time effect of the Earth’s motion. The instrumental differential B and V light and B-V color curves are shown in Figs 1 and 2. The photometric phases in Figs 1 and 2 are calculated by using the following light elements given by Çiçek, [10]:

HJD Min I JD = 2449162.4631(2) + 2 d .2509350(15) E.

(1)

2. Apsidal Motion Analysis During the observations of DR Vul, 12 primary and 7 secondary times of minima have been obtained by Çiçek, [11]. These minima have been presented in Table 2. Observed minima in different filters but in same epoch were averaged. The O-C values were calculated with the Eq. (1) using the following light elements given by Çiçek [11]. Observations of times of minima provide a simple method of determining the apsidal motion rate. For the eclipsing binaries with low orbital eccentricity, moments of the minima were given by Martynov [7], as follows: HJD Min = To + P.E + {± A cos( wo + w& E )},

(2)

where –A is for the primary minimum and E is integer, +A is for secondary minimum and E is halved, wo is the longitude of the periastron at an initial time and w& is the apsidal motion rate. The amplitude, A, in Eq. (2) is given by

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Figure 2. The light and color curves of DR Vul in 1994. Table 2. New photoelectric minima times of DR Vul.

A = Pe

(1 + cos ec 2 i) , 2π

(3)

where e is eccentricity and i is orbital inclination. To improve the apsidal motion parameters, the differential correction method was used. The light elements given by Khaliullina [6] were used as initial values. By applying Eq. (1) to primary and secondary times of minima simultaneously, new light elements of the system were obtained. The result is as follows:

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C. Çiçek / Apsidal Motion Problem in the Eclipsing Binary Star DR Vulpeculae

Figure 3. The O-C diagram for DR Vul.

HJD Min = 2446274 d .5038(10) + 2 d .25089080(32) E + 4.25(30)10 −9 E 2 ± 0.0701(7) cos(0 o.06076(34) E + 71o.30(81)) .

(4)

The computed O-C curves obtained with the above parameters are shown in Fig. 3. All times of minimum collected by Khaliullina [5], as well as the new ones given in Table 2, were used in this calculation. All Photoelectric and CCD times of minimum were used with a weight 1 in this computation. The current photographic data (as well as some of less precise measurements) were weighted with a factor of 0.2 while the earlier visual and photographic times of minimum were given a weight of 0.04 due to the large scatter in P gives the observed value of apsidal motion period to these data. The relation U obs = 360o w& be Uobs = 36.8 yr.

References [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12]

Hoeffmeister C. AN 1935; 225: 405. Tsesevich VP.), Astron. Tsirk. 1950; 100. Erloksova GE. Perem. Zvezdy 1959; 12: 298. Semeniuk I. AcA 1968; 18: 1. O’Connell JK. Ric. Astron. Specola Vaticana 1972; 8: 14. Khaliullina AI. DR Vulpeculae—the quadruple system. MNRAS 1987; 225: 425–36. Khaliullina AI, Khaliullin KhF. Photometric investigation of the eclipsing binary star DR VUL-orbital parameters and apsidal motion. AZh 1988; 65: 108–16. Wolf M, Diethelm R. Period changes in the eclipsing binary Dr-vulpeculae. MNRAS 1993; 263: 527. Wolf M, Diethelm R, Sarounova L. A&A 1999; 345: 553. Çiçek C. [Ph.D. Thesis]. 1995. Unpublished. Çiçek C. IAU IBVS 2001; 5142. Martynov DYa. ed. Zessewitch, Moscow: 1971; 325.

Perspectives in Astrobiology R.B. Hoover et al. (Eds.) IOS Press, 2005 © 2005 IOS Press. All rights reserved.

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Amino Acids: Probes for Life’s Origin in the Solar System Michael H. ENGELa, Vlad E. ANDRUSa and Stephen A. MACKOb a School of Geology & Geophysics, The University of Oklahoma Norman, Oklahoma 73019 USA b Department of Environmental Sciences, The University of Virginia Charlottesville, Virginia 22903 USA

Abstract. Several hundred amino acids have been identified in organisms, but only 20 are the building blocks of proteins. As best as can be determined from the fossil record, the 20 protein amino acids have never varied with respect to structure or stereochemistry. Approximately 55 amino acids that have yet to be discovered in modern terrestrial organisms have been identified in carbonaceous meteorites. If life originated on Earth, a fundamental question that remains to be answered is what were the source(s) and mechanisms of formation of the amino acids that preceded life? Laboratory simulation experiments have not resulted in the synthesis of all of the protein amino acids. Also, these experiments always produce racemic amino acids (D/L=1), whereas life as we know it is based almost exclusively on L-amino acids. The alternative to laboratory synthesis has been investigations of ancient rocks, terrestrial and extraterrestrial. Given that life is ubiquitous on present-day Earth and no rock is an entirely closed system, the challenge has been to distinguish ancient, indigenous amino acids from those more recently introduced via contact with the Earth’s biosphere. Amino acids in Precambrian rocks are not easily distinguished from modern overprints. However, amino acids in carbonaceous meteorites with short residence times on Earth provide a unique opportunity to begin to assess what the Earth’s organic inventory may have been like prior to life’s origin. In addition to numerous exotic amino acids, several of the common protein amino acids essential for life occur in the Murchison and Orgueil meteorites. More importantly, these amino acids exhibit the L-enantiomer excess that was, arguably, a necessary precondition for the origin of life. The stable isotope composition of amino acids in the Murchison meteorite confirms their authenticity. It is hypothesized that at least some of the starting materials for life on Earth may have been introduced by impact events. There are several protein amino acids that occur in all living organisms on Earth but have not been synthesized in the laboratory by abiotic mechanisms and have not been detected in carbonaceous meteorites. It is suggested that the presence of these amino acids, e.g.: Phe, Lys, His, and Arg, on other planetary bodies would by evidence for the existence of life as we know it.

Introduction Soils, sediments, and sedimentary rocks on Earth contain a variety of organic compounds derived primarily from the biosphere. Compounds whose origins can be traced back to specific organisms are called biomarkers. Thus, most compounds—such as amino acids, sugars, and fatty acids, the building blocks of proteins, carbohydrates, and lipids—are not, by definition, biomarkers. They are essential components of all organisms, past and present. A

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consequence of the ubiquitous nature of these compounds has been the extreme difficulty in distinguishing their origins in ancient materials. Given that all rocks and sediments are open systems, it is not yet possible to determine the extent to which organic compounds, such as amino acids, in ancient rocks are autochthonous or reflect a series of inputs from numerous sources with the passage of time. And, even if it were possible to establish that amino acids in ancient, Precambrian rocks, such as those in southern West Greenland, were the same age as the rocks in which they are contained, it is still not possible to establish whether these compounds formed by biotic or abiotic processes. The reasons for these uncertainties will be discussed below. Why amino acids, rather than other types of essential compounds, became the focus of attention for life’s origin may be attributed to a series of discoveries in the 1950s and early 1960s. Abelson [1] first reported the occurrence of amino acids in fossils. This discovery led to immediate speculation that it might be possible to begin to probe evolutionary change at the molecular level by establishing the amino acid sequences of proteins and peptides in fossils. At approximately the same time, Miller [2] reported that it was possible to synthesize amino acids from simple mixtures of inorganic compounds. This landmark discovery provided a possible mechanism for the synthesis of amino acids prior to life’s origin. The subsequent development of automated, liquid chromatographic methods for amino acid analysis [3,4] and gas chromatographic methods for determining amino acid stereochemistry [5,6] were quickly adopted for the analysis of fossil proteins and ancient sediments. Finally, the initial report by Nagy et al. [7] concerning hydrocarbons of biological origin in extraterrestrial materials, i.e.: the Orgueil meteorite, resulted in numerous early attempts to determine the distributions of amino acids in meteorites [8,9]. For the past forty years, scientists have continued to focus their attention on the distribution, stereochemistry, and more recently, the stable isotope composition of amino acids in ancient terrestrial and extraterrestrial materials with the hope of understanding how these compounds initially formed and subsequently became essential components of living organisms. The following discussion focuses on what is currently known about the occurrence of amino acids in ancient terrestrial and extraterrestrial materials and how this information may help us to understand life’s origin in the solar system.

1. Amino Acid Distributions 1.1. Terrestrial Materials There are 20 common, genetically encoded amino acids that are the building blocks of proteins in living organisms, past and present. For as far back in time as the fossil record enables us to determine amino acid composition, there is no indication that the structures of these building blocks have ever varied. While several hundred non-protein amino acids have been identified [10], their lower abundance and lack of preservation as components of common structural proteins greatly reduce the likelihood of their detection as indigenous components in older terrestrial materials. Amino acid distributions for specific proteins are often distinctive. However, even in well-preserved materials, distributions will change with the passage of time, owing to the decomposition of unstable amino acids, e.g.: Ser and Thr, and the formation of amino acids as the products of these decomposition reactions, e.g.: Gly, Ala, and Orn. For example, a comparison of amino acid constituents of shell protein for a modern Mercenaria shell with that of a well-preserved Pleistocene age Mercenaria shell are clearly similar (Fig. 1). However, it is also obvious that with the passage of time, the concentrations of Ser and Thr in the fossil shell have decreased. Given that amino acids such as Ser and Thr decompose

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Figure 1. Amino acid distributions in fossil (Pleistocene) and modern Mercenaria shells.

fairly rapidly, their presence in fossils or sediments older than a few million years is almost always attributed to recent contamination. However, the absence of these amino acids in older materials does not necessarily indicate a lack of contamination. Samples that are millions (or several billion) years old may have been contaminated multiple times in the past, with ample time for unstable amino acids to have decomposed subsequent to contamination. The oldest examples of sediments deposited by water are found at Isua in southern West Greenland (~3.8 Ga). While these sediments have undergone extensive metamorphism, it was reported that they contained microfossil and chemical evidence for ancient life [11]. More recently there have been reports that carbonaceous inclusions in apatite crystals in the Isua rocks may, based on their stable carbon isotope compositions, be relics of ancient life [12]. If true, this would mean that life existed on Earth as far back in time as the rock record is presently known to extend. Given the severity of impact events during the first 500–600 Ma of Earth history [13], the window of opportunity for life’s origin on Earth would seemingly have been restricted to less than a few tens of millions of years. The recent report that the Isua rocks may contain extraterrestrial material from impacts [14] further clouds the issue as to whether these rocks are true records of early Earth processes or a combination of extraterrestrial and terrestrial materials. Nagy et al. [15] determined the distribution of amino acids in interior samples of Isua banded ironstones. The distributions were similar to those found for lichens that were growing on some of the rock surfaces (Fig. 2). It is impossible to say whether a fraction of any individual amino acid was indigenous, but the distribution clearly indicates that the chances for contamination by encrusting biota are significant. Although these rocks have relatively low porosity and permeability, Engel [16] demonstrated that amino acids in aqueous solution can readily diffuse into the interior of these banded ironstones. As will be discussed in Section 1.2, the challenge that remains is to develop methods for distinguishing ancient from more recent organic matter in Precambrian rocks. 1.2. Extraterrestrial Materials As indicated above, attempts to determine the distribution of amino acids in carbonaceous meteorites began in the early 1960s. The results of these studies became suspect as it be-

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M.H. Engel et al. / Amino Acids: Probes for Life’s Origin in the Solar System

Figure 2. Amino acid distributions in Isua and lichens.

came apparent that the concentrations of amino acids in the samples were not much greater than those of the background levels in reagents, solvents, etc. that were available at that time [17]. Also, as in the case of the work of Nagy et al. [7] on Orgueil, there continued to be healthy skepticism concerning the possibility that samples of meteorites with extended residence times on Earth could have escaped contamination. Orgueil fell in France in 1864. Thus, almost 100 yr had elapsed from the time of its collection to the time of its analysis in the early 1960s. This is not to say that some of the compounds (amino acids, hydrocarbons, etc.) initially found in Orgueil and other carbonaceous meteorites were not indigenous. There just was no way at the time to prove that they were or were not. The fall of the Murchison meteorite in 1969 provided fresh extraterrestrial material for amino acid analysis by newly developed chromatographic and mass spectrometric methods. The majority of studies from 1969 to present have focused on various stones of Murchison since there were no additional observed falls of carbonaceous meteorites until the fall of the Tagish Lake meteorite in 2000. Shock and Schulte [18] reviewed the reported distributions of amino acids in stones of the Murchison meteorite. With the exception of one stone, the distributions of amino acids in the Murchison meteorite were consistent from laboratory to laboratory. Slight variations between laboratories were attributed to differences in the extraction efficiency of the methods employed. Typical amino acid distributions for the hydrolyzed water extract and the HCl extract of a Murchison meteorite stone subsequent to water extraction are shown in Fig. 3. Although up to 74 amino acids have been identified in the Murchison meteorite [19], several common protein and uncommon non-protein amino acids comprise the majority of this compound fraction, including α-aminoisobutyric acid (α-Aib), isovaline (Ival), βalanine (β-Ala), Gly, Ala, Asp, Glu, and Pro. The distribution of amino acids in similar extracts of the Orgueil meteorite [16] are also exotic, with Gly and β-Ala being major components (Fig. 3). Concentrations of major amino acid constituents of the water and HCl extracts of Murchison and Orgueil are listed in Table 1. Six protein amino acids (Phe, Tyr, Lys, His, Arg, and Trp) have never been detected in well-preserved stones of Murchison and Orgueil, and two others, Ser and Thr, have only been detected at trace levels [20]. This indicates that the stones have not been extensively contaminated during or subsequent to impact. It would be almost impossible to contaminate a meteorite with material of biological origin and not detect those amino acids.

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Figure 3. Amino acid distributions in meteorites. Table 1. Amino acid concentrations (nmolg-1) in water and acid extracts of Murchison and Orgueil meteorite stones [16].

Carbonaceous meteorites from Antarctica have been analyzed for amino acids [21–23]. However, the fact that Antarctic meteorites have extended residence times on Earth increases the chances for contamination. Many Antarctic stones exhibit weathering features [24]. Given the porous nature of carbonaceous meteorites, it stands to reason that prolonged exposure to Earth enhances the prospects for the diffusion of compounds into the stones. Amino acids are present in Antarctic ice [25,26]. A comparison of the protein amino acid distribution in the hydrolyzed water extract of an Antarctic stone [23] with that of a hydrolyzed sample of Antarctic ice core (Ross Ice Shelf) is shown in Fig. 4. All of the amino acids in Antarctic meteorites are unlikely to be the result of contamination. However, it is not possible to distinguish indigenous compounds from contamination based on abundance and distributions alone. 1.3. Simulation Experiments Numerous experiments have been attempted to simulate the synthesis of amino acids prior to life’s origin. Miller [27] provides a summary of the synthesis of protein and non-protein amino acids via spark discharge experiments. Khare et al. [28] synthesized amino acids

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Figure 4. Protein amino acid distributions in Antarctic ice and Yamato-74662. Table 2. Total concentration (nmol) of amino acids produced by spark discharge [30].

from inorganic precursor molecules using ultraviolet light as an energy source. Hennet et al. [29] synthesized amino acids under aqueous, hydrothermal conditions. It should be noted that none of these simulation experiments resulted in the synthesis of all of the protein amino acids or of the entire suite of non-protein amino acids detected in carbonaceous meteorites. However, as in the case of carbonaceous meteorites, simulation experiments result in the syntheses of large quantities of low-molecular-weight compounds, e.g.: Gly and Ala. Amino acid abundance decreases with increasing molecular complexity. In spark discharge experiments conducted by Engel et al. [30], Gly was an order of magnitude more abundant that any additional amino acids formed from the gaseous (ammonia, methane, hydrogen, and water) precursors (Table 2). This would be expected, assuming that higher molecular-weight compounds form from lower molecular-weight precursors. Whether any of these simulation experiments are indeed the actual pathways for the abiotic synthesis of life’s precursors on Earth or elsewhere is as yet unknown.

2. Amino Acid Stereochemistry 2.1. Terrestrial Materials One of the unique characteristics of life on Earth is that, owing to conformational constraints, the 20 genetically encoded amino acid constituents of proteins are almost exclu-

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Figure 5. Gas chromatograms of (a) amino acid extracts from an Isua rock and (b) lichen on the rock’s surface. Details of analytical procedures were previously reported by Engle [16].

sively of the L-configuration. Glycine is the exception since it does not contain an asymmetric center. Trace levels of D-amino acids occur in bacterial cell walls [31]. They may also occur in living organisms at trace levels via racemization [32] subsequent to synthesis. However, upon death, D-amino acids represent an increasing percentage of residual proteins and peptides, the extent to which is largely dependent on the environment of preservation [33] and diagenetic reactions, [33,34]. While amino acids racemize at different rates, in theory, most amino acids in fossil proteins and peptides should be racemic, i.e.: D/L=~1.0, after several million years. However, given that racemization rates are dependent on temperature, pH, the presence of water, etc., it is conceivable that non-racemic amino acids may persist under extreme conditions of preservation (in particular if a protein retains its initial structural integrity). Also, residual peptides and amino acids may become incorporated in geomacromolecules, e.g.: humates and kerogens, during diagenesis, and it has been clearly shown that subsequent to incorporation, racemization may cease [34]. Since racemization is theoretically complete in a few million years under “normal” preservation conditions, it would be expected that autochthonous amino acids in ancient sediments should be racemic, or approximately so. This is rarely if ever the case. In addition to the fact that racemization may be hindered by incorporation into macro-molecular materials, rocks and sediments are open systems. Thus, with the passage of time, amino acids are introduced into older rocks by the migration of fluids, e.g.: meteoric waters and basinal brines. For example, the amino acids in the Isua rocks are not racemic, with L-amino acids present in excess (Fig. 5). While a percentage of these amino acids may have either formed by biotic or abiotic processes at the time the Isua sediments were deposited, clearly, subsequent events have resulted in the introduction of additional L-amino acids. As indicated above, lichens presently growing on the rocks are one possible source of contamination (Fig. 5). But additional episodes of contamination may have occurred prior to this. Also, the fact that the Isua rocks have been metamorphosed, implies that their present-day amino acid constituents are unlikely to be remnants of abiotic or biological processes at the time of deposition ~3.8 Ga ago.

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Table 3. Amino acid D/L values for sequential extractions of a Murchison stone [38].

In summary, the Isua rocks represent a classic case of the challenges confronting scientists attempting to study the early history of organic compound synthesis on Earth. As will be discussed below, amino acids synthesized by abiotic processes are racemic. However, biologically-formed amino acids racemize with the passage of time. Thus, in older rocks, it is uncertain whether the occurrence of racemic amino acids was a consequence of one pathway or the other or a combination of both. Similarly, non-racemic amino acids may indicate subsequent inputs, but they do not preclude the possibility that some of the amino acids in the rock are indigenous. It is not possible to make this distinction at this time. 2.2. Extraterrestrial Materials It is generally assumed that amino acids in carbonaceous meteorites formed by abiotic processes. As will be discussed below, simulation experiments for the abiotic synthesis of amino acids result in the formation of racemic mixtures. Thus, from a historical perspective, it was assumed early on that indigenous amino acids in carbonaceous meteorites would be racemic. In cases where the D/L value for an amino acid was <1.0, i.e.: an Lexcess, this was attributed to contamination by the Earth’s biosphere at the time of or subsequent to impact [26]. It has also been recently suggested [35] that in some cases an Lenantiomer excess might be a consequence of the co-elution of another compound with the L-enantiomer, thus increasing its observed peak area. However, the fact that there have been relatively few published chromatograms documenting the stereochemistry of amino acids in carbonaceous meteorites has hindered progress in this important area of research. Kvenvolden et al. [36] were the first to determine the stereochemistry of amino acids in the Murchison meteorite. They reported that alanine was approximately racemic. However, their inability to monitor selected ions characteristic of the amino acid made it impossible at that time to verify the actual D/L value. Engel and Nagy [37] reported that several common protein amino acids in the hydrolyzed water extract of a Murchison meteorite stone were not racemic (L-enantiomer excess). They used selected ion monitoring to confirm that the D/L values were <1.0. More intriguing was the observation by Engel and Nagy [37] that amino acids recovered by acid hydrolysis of the residual Murchison stone subsequent to water extraction were even less racemized. Silfer [38] digested the residual mineral phase of a Murchison stone with HF subsequent to initial extractions with water and HCl and observed that the amino acids recovered by this third extraction step were even less racemized (Table 3). If the Murchison meteorite stones were superficially contaminated by amino acids during impact or subsequent collection, the amino acid contaminants should have been removed by the initial water and/or HCl extraction steps. More recently, Engel and Macko [20] published additional ion chromatograms documenting that common protein amino acids in extracts of the Murchison meteorite are non-racemic. There have been relatively few recent investigations of the stereochemistry of amino acids in carbonaceous meteorites other than Murchison. Ehrenfreund et al. [39] reported the abundances of the D- and L-enantiomers of several amino acids in CI (Orgueil and Ivuna) and CM (Murchison and Murray) carbonaceous meteorites. However, they determined

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Table 4. Bulk organic stable isotope compositions of carbonaceous meteorites.

amino acid abundances by high-performance liquid chromatography and provided no mass spectrometric confirmation of the amino acid identities or confirmation of the D/L values by selected ion monitoring. Thus, their observations concerning stereochemistry remain unverified. It is interesting to note, however, that their report of racemic Ala in the hydrolyzed water extract of the Orgueil meteorite is in agreement with the previous finding of Engel [16], the latter being confirmed by mass spectrometry. However, Engel [16] also reported that Ala was not racemic in the subsequent acid hydrolyzate of the residual mineral phase of Orgueil (L-enantiomer excess). The stereochemistry of Ala in the Murchison meteorite has been the focus of much attention, largely because of its abundance and the facility by which the enantiomers can be resolved. However, it should be noted that racemic alanine can form via the decomposition of other amino acids [40]. Thus, it is possible that the D/L values reported for Ala in various stones of the Murchison meteorite are not the authentic values. This might also explain why Ala is more highly racemized than the other amino acids in Murchison and Orgueil. 2.3. Simulation Experiments While it has been long assumed that the abiotic synthesis of amino acids results in racemic mixtures, it was not until the 1960s that the technology became available to accurately determine the stereochemistry of amino acids. In fact, there have only been a few published reports documenting the stereochemistry of amino acids synthesized by laboratory simulation experiments in which gas chromatography/mass spectrometry was used to confirm the D/L values. For example, Khare et al. [28] reported that amino acids in extracts of tholins synthesized using ultraviolet light as an energy source were racemic. Similarly, Muñoz Caro et al. [41] reported the synthesis of racemic amino acids by ultraviolet irradiation of interstellar ice analogs. Hennet et al. [29] synthesized racemic amino acids under hydrothermal conditions and Engel et al. [30] reported the synthesis of racemic amino acids by spark discharge. The implication of these findings with respect to the report of non-racemic amino acids in carbonaceous meteorites by Engel and colleagues [20,25,37,42–44] is discussed in Section 4.

3. Stable Isotope Composition of Amino Acids in Carbonaceous Meteorites The absence of several amino acids, which are common protein constituents, in the Murchison meteorite is compelling evidence for the authenticity of the compounds that are present. It would be almost impossible to selectively introduce some amino acids and not the others during impact and/or subsequent collection, storage, and analysis. The excess of the Lamino acid enantiomers in the Murchison extracts [20,25,37,42–44] was, however, such a potentially important observation with respect to life’s origin, that an independent method for verifying their authenticity was sought. The bulk organic matter in carbonaceous meteorites is enriched in 13C and 15N relative to organic matter on Earth (Table 4). Similarly, Epstein et al. [45] reported that the stable carbon and nitrogen isotope values for the total amino acid fraction of the Murchison mete-

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Table 5. Stable isotope values for amino acids in the Murchison meteorite [42,44].

orite were enriched in 13C and 15N (23.1 and 90.0‰, respectively) relative to amino acids of biological origin on Earth. Based on this information, Engel and Macko [46,47] proposed that it should be possible to determine the extent to which amino acids in the Murchison meteorite were indigenous as opposed to terrestrial overprints based on the stable isotope composition of their respective enantiomers. Assuming that the D- and L-enantiomers of an amino acid were formed by the same abiotic mechanism, they should, in theory have identical stable isotope compositions. In support of this hypothesis, Engel et al. [30] have shown that the stable carbon isotopes of the D- and L-enantiomers of Asp and of Ala formed by spark discharge are identical. If the L-enantiomer excess in the Murchison meteorite is a consequence of terrestrial contamination, then the L-enantiomer should be depleted in 13C and 15N relative to the D-enantiomer. Engel and Macko [47] have also shown that amino acids retain their stable carbon and nitrogen isotopic integrity during racemization. Thus, in any systems where partial racemization occurred, the isotope compositions of the respective enantiomers of an amino acid should remain the same, provided once again that there have been no exogenous inputs or kinetic isotope effects associated with the preferential reaction of one enantiomer relative to the other. Engel et al. [48] first documented the utility of this approach by determining the authenticity of amino acid enantiomers in fossil shells. The methodology for determining the stable carbon and nitrogen isotope compositions of amino acid enantiomers at low abundance levels using gas chromatography/combustion/isotope ratio mass spectrometry is reported elsewhere [49,50]. As can be seen in Table 5, the stable carbon and nitrogen isotope compositions of the amino acids in the Murchison meteorite are moderately to substantially enriched in 13C and 15 N relative to amino acid constituents of organisms on Earth. The stable carbon and nitrogen isotope compositions of the Earth’s biomass reflect fractionations that occur with primary production, largely a consequence of kinetic isotope effects associated with reactions such as photosynthesis. Subsequent fractionations result from the multitude of biosynthetic pathways in living organisms. These fractionations are preserved in heterotrophs, which reflect the isotopic compositions of their diets, plus or minus a few per mil [51,52]. Also, organic matter preserved in fossils and sedimentary rocks tends to retain the stable isotope composition of the biomass from which it is derived. In general, the range in δ13C and δ15N values for organic matter on Earth are approximately –10 to –40‰ and –10 to +10‰, respectively. Clearly, the stable isotope values for the amino acids in the Murchison meteorite are outside of these ranges. For amino acids in which stable isotope values could be determined for their respective D- and L-enantiomers, the values are, within experimental error, indistinguishable. This would not have been the case if the L-enantiomer excess were a consequence of contamina-

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tion by biological materials. Pizzarello and Cronin [35] have suggested an alternative scenario invoking the co-elution of other compounds in the Murchison meteorite with the Lenantiomers. However, the probability of each L-enantiomer in Murchison co-eluting with a compound having a similar mass spectrum and identical carbon and nitrogen isotopic compositions is remote if not impossible. Thus, the stable isotope data confirm our initial conclusions based on the absence of specific protein amino acids in Murchison. That is, the L-excess is an authentic characteristic of the Murchison meteorite and is likely to be an authentic characteristic of the Orgueil meteorite as well.

4. Conclusions Assuming that life originated on Earth, it is highly unlikely that the precursors for this event were racemic or that homochirality emerged by random event(s) during the earliest stages of life’s origin [53,54]. There have been no successful experiments for the abiotic synthesis of non-racemic amino acids under early Earth conditions, although the recent report by Hazen et al. [55] on selective adsorption of D- an L-enantiomers on mirror-related crystal growth surfaces of calcite certainly merits further investigation. Our observation that amino acids in carbonaceous meteorites exhibit a moderate to strong excess of their respective Lenantiomers provides an alternative source for homochirality that preceded life’s origin on Earth, i.e.: impact events during the first few hundred million years subsequent to the formation of the planet. The question is, why do amino acids in extraterrestrial materials, such as carbonaceous meteorites, exhibit this L-excess? At first glance, the obvious suggestion might be that the meteorites contain vestiges of life from elsewhere in the solar system. However, the fact that several protein amino acids are not present in the carbonaceous meteorites suggests that these materials are not relics of life as we know it. It is possible that their absence is a consequence of differences in stability, but this hypothesis is as yet untested. An alternative explanation is that the amino acids in carbonaceous meteorites were initially racemic and that the L-excess is a consequence of abiotic processes that resulted in the preferential destruction of the D-enantiomers [54,56–58]. Several protein amino acids, including Phe, Arg, Lys, and His, are present in all organisms on Earth. These amino acids have never been synthesized in simulation experiments and have not been detected in carbonaceous meteorites. The presence of these amino acids on another planetary body, such as Mars, would be a strong indicator for the previous existence of life. The challenge will be to avoid contamination of the Martian surface with amino acids from Earth during sample collection. Given the likelihood that organic compounds formed on Mars will be isotopically distinct from those on Earth, compound specific stable isotope analysis should prove useful for documenting the authenticity of these compounds if they are present.

References [1] Abelson PH. Organic constituents of fossils. Carnegie Inst. Wash. Year Book 1954; 53: 97–101. [2] Miller SL. Production of amino acids under possible primitive earth conditions. Science 1953; 117: 528–9. [3] Spackman DH, Stein WH, Moore S. Automatic recording apparatus for use in the chromatography of amino acids. Anal. Chem., 1958; 30: 1190–206. [4] Hamilton PB. Ion exchange chromatography of amino acids: a single column, high resolving, fully automatic procedure. Anal. Chem., 1963; 35: 2055–64. [5] Charles R, Fischer G, Gil-Av E. Resolution of (±) 2-n-alkanols by gas-liquid partition chromatography. Isr. J. Chem. 1963; 1: 234–5.

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[6] Pollock GE, Oyama VI, Johnson RO. Resolution of racemic amino acids by gas chromatography. J. Gas Chromatogr. 1965; 3: 174–6. [7] Nagy B, Meinschein WG, Hennessy DJ. Mass spectrometric analysis of the Orgueil meteorite: evidence for biogenic hydrocarbons. Ann. NY Acad. Sci. 1961; 93: 25–35. [8] Degens ET, Bajor, M. Amino acids and sugars in the Bruderheim and Murray meteorites. Naturwiss. 1962; 49: 605–6. [9] Kaplan IR, Degens ET, Reuter JH. Organic compounds in stony meteorites”, Geochim. Cosmochim. Acta, 1963; 27: 805–34. [10] Hunt S. The non-protein amino acids. In: Barrett GC, editor. Chemistry and biochemistry of the amino acids. London: Chapman and Hall; 1985, p. 55–138. [11] Pflug HD, Jaeschke-Boyer H. Combined structural and chemical analysis of 3,800-Myr-old microfossils. Nature 1979; 280: 483–6. [12] Mojzsis SJ, Arrhenius G, McKeegan KD, Harrison TM, Nutman AP, Friend RL. Evidence for life on Earth before 3,800 million years ago. Nature 1996; 384: 55–9. [13] Chyba CF, Sagan C. Endogenous production, exogenous delivery and impact shock synthesis of organic molecules: an inventory for the origins of life. Nature 1992; 355: 125–32. [14] Schoenberg R, Kamber BS, Collerson KD, Moorbath S. Tungsten isotope evidence from ~3.8-Gyr metamorphosed sediments for early meteorite bombardment of the Earth. Nature 2002; 418: 403–5. [15] Nagy B, Engel MH, Zumberge JE, Ogino H, Chang SY. Amino acids and hydrocarbons in the ~3,800Myr old Isua rocks, southwestern Greenland. Nature 1981; 289: 53–6. [16] Engel MH. [Ph.D. thesis]. Tucson (AZ): The University of Arizona; 1980. [17] Hayes JM. Organic constituents of meteorites. Geochim. Cosmochim. Acta 1967; 31: 1395–440. [18] Shock EL, Schulte MD. Summary and implications of reported amino acid concentrations in the Murchison meteorite. Geochim. Cosmochim. Acta, 1990; 54: 3159–73. [19] Cronin JR, Pizzarello S, Cruikshank DP. Organic matter in carbonaceous chondrites, planetary satellites, asteroids and comets. In: Kerridge JF, Matthews MS, editors. Meteorites and the early solar system. Tucson: University of Arizona Press; 1988. p. 819–57. [20] Engel MH, Macko SA. The stereochemistry of amino acids in the Murchison meteorite. Precambrian Res. 2001; 106: 35–45. [21] Kotra RK, Shimoyama A, Ponnamperuma C, Hare PE. Amino acids in a carbonaceous chondrite from Antarctica. J. Mol. Evol. 1979; 13: 179–84. [22] Cronin JR, Pizzarello S, Moore CB. Amino acids in an Antarctic carbonaceous chondrite. Science 1979; 206: 335–7. [23] Shimoyama A, Ponnamperuma C, Yanai K. Amino acids in the Yamato carbonaceous chondrite from Antarctica. Nature 1979; 282: 394–6. [24] Welten KC. Concentrations of siderophile elements in nonmagnetic fractions of Antarctic H- and Lchondrites: A quantitative approach on weathering effects. Meteoritics and Planet. Sci. 1999; 34: 259–70. [25] Engel MH, Macko SA. Stable isotope analysis of amino acid enantiomers in the Murchison meteorite at natural abundance levels”, In: Hoover RB, editor. Instruments, methods, and missions for the investigation of extraterrestrial microorganisms. Proc. SPIE 1997; 3111: 82–5. [26] Bada JL, Glavin DP, McDonald GD, Becker L. A search for endogenous amino acids in Martian meteorite ALH84001. Science 1998; 279: 362–5. [27] Miller SL. The prebiotic synthesis of organic compounds on the early Earth. In: Engel MH, Macko SA, editors. Organic geochemistry: principles and applications. New York: Plenum Press; 1993. p. 625–37. [28] Khare BN, Sagan C, Ogino H, Nagy B, Er C, Schram KH, Arakawa ET. Amino acids derived from Titan tholins. Icarus 1986; 68: 176–84. [29] Hennet RJ-C, Holm NG, Engel MH. Abiotic synthesis of amino acids under hydrothermal conditions and the origin of life: a perpetual phenomenon? Naturwiss. 1992; 79: 361–5. [30] Engel MH, Macko SA, Qian Y, Silfer JA. Stable isotope analysis at the molecular level: A new approach for determining the origins of amino acids in the Murchison meteorite. Adv. Space. Res. 1995; 15: 99–106. [31] Perry RS, Engel MH, Botta O, Staley JT. Amino acid analyses of desert varnish from the Sonoran and Mojave Deserts. Geomicrobiology 2003; in press. [32] Helfman PM, Bada JL. Aspartic acid racemization in tooth enamel from living humans. Proc. Natl. Acad. Sci. U.S.A. 1975; 72: 2891–4. [33] Goodfriend GA, Collins MJ, Fogel ML, Macko SA, Wehmiller JF, editors. Perspectives in amino acid and protein geochemistry. New York: Oxford University Press; 2000. [34] Rafalska JK, Engel MH, Lanier WP. Retardation of racemization rates of amino acids incorporated into melanoidins. Geochim. Cosmochim. Acta 1991; 55: 3669–75. [35] Pizzarello S, Cronin JR. Alanine enantiomers in the Murchison meteorite. Nature 1998; 394: 236.

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[36] Kvenvolden KA, Lawless J, Pering K, Peterson E, Flores J, Ponnamperuma C, Kaplan IR, Moore C. Evidence for extraterrestrial amino acids and hydrocarbons in the Murchison meteorite”, Nature 1970; 228: 923–6. [37] Engel MH, Nagy B. Distribution and enantiomeric composition of amino acids in the Murchison meteorite”, Nature 1982; 296: 837–40. [38] Silfer JA. [Ph.D. Thesis]. Norman (OK): University of Oklahoma; 1991. [39] Ehrenfreund P, Glavin DP, Botta O, Cooper G, Bada JL. Extraterrestrial amino acids in Orgueil and Ivuna: Tracing the parent body of CI type carbonaceous chondrites. Proc. Natl. Acad. Sci. U.S.A. 2001; 98: 2138–41. [40] Engel MH, Hare PE. The condensation of amino acids and sugars: An evaluation of stereochemistry, decomposition and rearrangement reactions. Carnegie Inst. Wash. Year Book 1982; 81: 425–30. [41] Muñoz Caro GM, Meierhenrich UJ, Schutte WA, Barbier B, Arcones Segovia A, Rosenbauer H, Thiemann WH-P, Brack A, Greenberg JM. Amino acids from ultraviolet irradiation of interstellar ice analogs. Nature 2002; 416: 403–6. [42] Engel MH, Macko SA, Silfer JA. Carbon isotope composition of individual amino acids in the Murchison meteorite. Nature 1990; 348: 47–9. [43] Engel MH, Macko SA, Nagy B. The organic geochemistry of carbonaceous meteorites: amino acids and stable isotopes. In: Engel MH, Macko SA, editors. Organic geochemistry, principles and applications, Plenum Press: 1993. p. 685–95. [44] Engel MH, Macko SA. Isotopic evidence for extraterrestrial non-racemic amino acids in the Murchison meteorite. Nature 1997; 389: 265–8. [45] Epstein S, Krishnamurthy RV, Cronin JR, Pizzarello S, Yuen GU. Unusual stable isotope ratios in amino acid and carboxylic acid extracts from the Murchison meteorite. Nature 1987; 326: 477–9. [46] Engel MH, Macko SA. The separation of amino acid enantiomers for stable carbon and nitrogen isotope analyses. Anal. Chem. 1984; 56: 2598–600. [47] Engel MH, Macko SA. Stable isotope evaluation of the origins of amino acids in fossils. Nature 1986; 323: 531–3. [48] Engel MH, Goodfriend GA, Qian Y, Macko SA. Indigeneity of organic matter in fossils: A test using stable isotope analysis of amino acid enantiomers in Quaternary mollusk shells. Proc. Natl. Acad. Sci. U.S.A. 1994; 91: 10475–8. [49] Silfer JA, Engel MH, Macko SA, Jumeau EJ. Stable carbon isotope analysis of amino acid enantiomers by conventional isotope ratio mass spectrometry and combined gas chromatography/isotope ratio mass spectrometry. Anal. Chem. 1991; 63: 370–4. [50] Macko SA, Uhle ME, Engel MH, Andrusevich VE. Stable nitrogen isotope analysis of amino acid enantiomers by gas chromatography/combustion/isotope ratio mass spectrometry. Anal. Chem. 1997; 69: 926–9. [51] DeNiro MJ, Epstein S. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 1978; 42: 495–506. [52] DeNiro MJ, Epstein S. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta 1981; 45: 341–51. [53] Goldanskii VI, Kuzmin VV. Chirality and the cold origin of life. Nature 1991; 352: 114. [54] Bonner WA. The origin and amplification of biomolecular chirality. Orig. Life Evol. Biosphere 1991; 21: 59–111. [55] Hazen RM, Filley TR, Goodfriend GA. Selective adsorption of L- and D-amino acids on calcite: Implications for biochemical homochirality. Proc. Natl. Acad. Sci. U.S.A. 2001; 98: 5487–90. [56] Greenberg JM. Prebiotic chiral molecules created in interstellar dust and preserved in comets, comet dust, and meteorites: an exogenous source of life’s origins. In: Hoover RB, editor. Instruments, methods and missions for the investigation of extraterrestrial microorganisms. Proc. SPIE 1997; 3111: 226–37. [57] Bailey J, Chrysostomou A, Hough JH, Gledhill TM, McCall A, Clark S, Ménard F, Tamura M. Circular polarization in star-formation regions: Implications for biomolecular homochirality. Science 1998; 281: 672–4. [58] Rikken GLJA, Raupach E. Enantioselective magnetochiral photochemistry. Nature 2000; 405: 932–5.

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Mineralization of Cyanobacteria L. GERASIMENKO, V. ORLEANSKY and L. ZAITSEVA Institute of Microbiology of RAS, Prospect 60-letya Octyabrya 7/2, Moscow, 117812, Russia Abstract. Mineralization (silification, carbonatization and phosphatization) of cyanobacteria was studied in nature and laboratory. The increase in concentration of silica, phosphates, carbonates, and calcium leads to a sequence of morphological changes of cyanobacteria: (1) Formation of slime sheath, (2) formation of isolated globules of minerals on the slime sheath, (3) mineralization of slime sheaths of viable cells, and (4) mineralization of trichomes of dead cells.

Cyanobacteria are ancient organisms that were surprisingly stable over the entire evolution of life on Earth. The similarity of organic remains from ancient stromatolites, oncolites, and phosphorites to extant cyanobacteria [1–3] suggests the predominant role of these photosynthetic organisms in biogenic carbonates deposition. Accordingly, the observation of the mineralization processes in nature and laboratory experiments allows us to understand cyanobacterial activity in the geological past. Cyanobacteria, together with other bacteria, form microbial communities that dominated Earth for over 3 billion years and were responsible for important geological processes, including the accumulation of many sedimentary rocks and mineral resources. However, eukaryotic organisms pushed cyanobacteria from epicontinental marine basins to ecological niches, often with extreme conditions: hyperhaline lagoons of the sea, soda lakes, and hot springs, where thermophilic, halophilic, and alkaliphilic microbial communities survive even today. Thermophilic communities were observed in the caldera of the volcano, Uzon, in Kamchatka and Kuril Islands; halophilic communities, in the lagoons of Sivash in Crimea; and alkaliphilic communities in soda lakes in Siberia. In hot springs with a large content of silica, the community is partly mineralized (Fig. 1(a) and (b)). These siliceous crusts contain mineralized microbial remains, i.e.: modern microfossils [4]. Different stages of silification were found in these crusts (Fig. 1(c)). The process of mineralization begins with the penetration of silica within the cell and precipitation of minute globules on the cell walls. During the next stage, globules fuse into a single crust surrounding the cell. The external surface of the cells is smooth, while the internal surface is globular. Later, opal globules fill the spaces between and within the filaments until completely silicified rock is formed. In the laboratory, it was shown that penetration of silica occurs only after the cell’s death. Living cells have mechanisms of precluding high silica concentrations, namely the formation of the thick slime sheaths. The thermophilic and halophilic mats often contain carbonate inclusions represented by aragonite and calcite. Cyanobacteria observed in these mats are also carbonatized. The rigid correlation between the content of cyanobacteria in the mat [5] indicates that one of the reasons is the alkalization of the media resulting from the active photosynthesis of cyanobacte-

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Figure 1. Natural mineralized mat (Kamchatka): (a) Modern stromatolite, Bar=20 sm; (b) cross section of stromatolite, Bar=2 sm; (c) mineralized cyanobacterium Mastigocladus laminosus, Bar=5 μm; and (d) mineralogy of mat.

ria. Laboratory experiments show that the precipitation of carbonates reaches its maximum when photosynthetic conditions are optimal [6]. The increase in the content of calcium++ (Ca++) and carbonates in the medium results in morphological changes, primarily in the formation of slime sheaths. Later Ca-carbonate globules precipitate on sheaths of living cells and gradually mineralized the entire trichomes of dead cells. Experimental data show that some content of carbonates or carbon dioxide (CO2) in the media plays a decisive inhibiting effect on the growth of cyanobacteria. High concentrations of carbonates increase the pH of the medium to >11; and high concentrations of CO2 decrease the pH to <5. The cells die and mineralization of trichomes occurs. The action of phosphorus on the growth and mineralization of cells was studied carefully. Our experiments showed that halophilic cyanobacteria—Microcoleus chthonoplastes, the dominant organism of cyanobacterial mats—can survive in a wide range of inorganic phosphorus concentrations. However, irrespective of concentrations, the active re-

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Figure 2. Formation of mineral microtubes of fluorine-apatite. Bar=1μm.

moval of phosphorus from the medium was observed in the first 3 hr and was completed in 24 hr [7,8]. Experiments showed that not all phosphorus penetrated the cell, the larger part of it was absorbed on the surface. The higher its concentration in the medium, the more intensive is the absorption. The active influx of phosphorus into the cell occurs by its active transport through the membrane. It accumulates in larger quantities than outside the cell, and its concentration there is higher than the cell requires for its metabolism. In Microcoleus chthonoplastes, the active transport occurs with a maximum rate in the first 3 min of contact. In 3 days, a two-fold decrease in rate was observed. Phosphorus can be stored in microbial cells in the form of inorganic polyphosphates that serve as a phosphorus reserve to provide for cell survival under phosphorus starvation. Various fractions of polyphosphates may respond differently to changes in the environment. Fractional distribution of the phosphates in cyanobacteria grown in the presence of different concentrations of polyphosphates corresponded to morphological alterations in the cells related to their mineralization. The superficial accumulation of acid-insoluble polyphosphates, localized close to the cell surface, stimulated the mineralization of slime sheaths. Under a high concentration of phosphorus (lethal for cells) the accumulation of orthophosphates and nucleoside phosphates was observed. This is when mineralization of trichomes begins [8]. The x-ray investigation of mineral sheaths and trichomes showed that the emerging, poorly crystallized phosphate minerals of the apatite group have a major diffractionary maximum that is close to francolite [7]. To obtain a crystallized apatite in the laboratory, NaF was added to the medium since F is an isomorphic element of the apatite structure [9]. The solid precipitate was studied with scanning electron microscopy, and electron micrographs showed dispersive-lay spherulite-like particles on which there were well-ordered microtubes (Fig. 2). They may be situated on or in the precipitate, near trichoms or on them. The microtubes ranged in diameter from 0.8 to 1.1 μm, and their length varied from 1.0 to 12.0 μm. Microtubes consist of small, individual, especially smooth spherulites of 0.2–0.5 μm, and the spherulites may be densely packed. The observed mineral microtubes resemble modern and ancient microfossils by their gross morphology. Thus, the data presented show that in some cases, filamentous or tubular structures may not represent the fossilized microorganism itself. That is why it is necessary to be careful in their interpretation. Thus, the action of different ions on cells is similar in spite of the fact that phosphorus, calcium, and carbonate are necessary components for the growth of all cyanobacteria, but silica is a necessary element only for specific groups of alga. The increase in concentration of these components leads to morphological changes of the cells (Fig. 3), which are: 1. The surface of the cells becomes covered with a slime sheaths. This sheath may be twice as thick as the trichomes. The appearance of this sheath in cyanobacteria and many other microorganisms indicates an unfavorable environment and is a cellular

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Figure 3. Different stages of mineralization of cyanobacteria. (a) Viable trichomes of Microcoleus chthonoplastes, (b) slime sheaths, (c) viable trichomes glide from mineral sheath, (d) mineralized sheath. Bar=3 μm.

response for its protection. The sheath consists of an amorphous substance containing polysaccharide microfibrils as a matrix. The latter may become a center of a mineralization process in that they form mineral microtubes around the cyanobacterial filaments. 2. As ion concentration increases, isolated mineral globules precipitate on the sheaths, then emerge in them. Later they fuse on larger bodies and finally form a complete mineral sheath. Mineral accumulation occurs only in the slime sheath and does not involve trichomes. Cells remain viable, and occasionally, it was observed that trichomes move out of the mineral covering leaving an empty tube behind. 3. As concentration increases, the culture dies, and the trichome itself becomes mineralized. Large rates of absorption in first few minutes explain the good preservation of morphological structures of cyanobacteria in ancient rocks.

Acknowledgments This work was supported in part by the Russian Foundation for Basic Research, projects NoNo 00–05–64603, 02–04–48094, and INTAS 97–30776.

References [1] Rozanov AYu, Zhegallo EA. Problem of origin of ancient phosphorites of Asia. Lithology and Mineral Resources 1989; 3: 62–82. [2] Stal LJ. Cyanobacterial mats and stromatolites. In: Whitton BA, Potts M, editors. The Ecology of Cyanobacteria. The Netherlands: Kluver Academic Publishers; 2000. p.61–120. [3] Riding RE, Awramik SM. Microbial sediments. Berlin-Heidelberg-New York: Springer-Verlag; 2000. [4] Krilov IN, Orleansky VK, Tichomirova NS. Silification: everlasting preparations. Priroda 1989; 4: 4–12. [5] Zavarzin GA, editor. Calderic microorganisms. Moscow: Nauka; 1989. [6] Nekrasova VK, Gerasimenko LM, Romanova AK. Physiological especially of photosynthesis of Mastigocladus laminosus. Microbiology 1983; 52 (4): 549–51. [7] Gerasimenko LM, Goncharova IV, Zhegallo EA, Rozanov AYu, Ushatinskaya GT. Proccess of mineralization (phosphatization) of cyanobacteria. Litology and Mineral Resources 1996; 2: 208–14.

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[8] Gerasimenko LM, Goncharova IV, Zaitseva LV. The affect of P-content on the growth and mineralization of cyanobacteria. Microbiology 1998; 67 (2): 254–9. [9] Goncharova IV, Gerasimenko LM, Zavarzin GA, Ushatinskaya GT. Formation of mineral phosphate microtubes. Current Microbiology 1993; 27: 187–90.

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Microfossils, Biominerals, and Chemical Biomarkers in Meteorites Richard B. HOOVER Astrobiology Group Leader, Space Science Department/SD50 NASA George C. Marshall Space Flight Center, Huntsville, AL 35812 Abstract. The detection of biominerals, chemical biomarkers, and putative microfossils in the Mars meteorite, ALH84001, stimulated the newly emerging fields of astrobiology and bacterial paleontology. The debate triggered by the ALH84001 results highlighted the importance of developing methodologies for recognizing chemical biomarkers, biominerals, and microfossils in living and fossilized bacteria in ice, permafrost, rocks, meteorites, and other astromaterials prior to the return of samples from comets, asteroids, and Mars. Comparative studies of the chemical, mineral, and morphological biomarkers in living and fossil microorganisms are essential to developing the expertise needed to differentiate biogenic forms from abiotic microstructures and to recognize indigenous biosignatures and distinguish them from recent biological contaminants. At the NASA Marshall Space Flight Center (MSFC) and the Paleontological Institute of the Russian Academy of Sciences (PIN/RAS), ultrahigh-resolution imaging and x-ray elemental analysis has been carried out on living bacteria, ancient microbes cryopreserved in ice and permafrost, biominerals and microfossils in a wide variety of rocks and meteorites. The environmental scanning electron microscope (ESEM) and field emission scanning electron microscope (FESEM) studies have resulted in the detection of a large number of indigenous biomarkers and lithified or carbonized microfossils found embedded in situ in the rock matrix of carbonaceous meteorites. Many of these forms are similar to microfossils and biominerals seen in living and fossil magnetotactic bacteria and cyanobacteria from hypersaline soda lakes; phosphorites of Khubsugul, Mongolia; and high carbon rocks of the Siberian and Russian Platforms. Some of the assemblages of microfossils in carbonaceous meteorites exhibit consistent consortia and microbial ecosystems. Many of the forms are large and extremely complex, exhibiting recognizable nanostructures, such as flagella, spines, biofilms, apical cells, and reproductive stages (trichomes, spores, akinetes, and hormogonia) such as are known in modern Nostocacean cyanobacteria. A review of the prior studies and recently obtained images, and x-ray data from a wide variety of carbonaceous meteorites and terrestrial rocks is provided herein.

Introduction The discovery by McKay et al. [1] of chemical biomarkers and possible microfossils in an ancient meteorite from Mars, ALH84001, initiated the field of astrobiology and renewed a scientific debate that highlighted the need to develop bioindicators and biomarkers for recognition of traces of life in the cosmos. The minute (100–400 nm) dimensions of the putative nanofossils in ALH84001 (Fig. 1 (a)) triggered a debate on the size limitations of microbial life on Earth. It has subsequently been shown that living on Earth there are dwarf

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Figure 1. (a) Putative 400-nm nanofossils in ALH84001 and (b) a novel motile archaeon (120- to 400-nm diameter) from the Rainbow deep sea hydrothermal vent.

bacteria, nanofossils, nanobacteria, and nanocells [2–7] and a nanoarchaeon symbiont [8] that have sizes comparable to the possible nanofossils of ALH84001. (Fig. 1 (b)) At MSFC, a minute anaerobic hyperthermophile from the Rainbow deep-sea hydrothermal vent (Fig. 1 (b)) was isolated. This autonomous obligate sulfurophile is growing in pure culture and motile with flagella. These coccoidal microbes exhibit a very wide size distribution, ranging from individuals with a diameter of ~100 nm or less to forms as large as 1 δm. Even though the lower limit on the size of autonomous microbial life on Earth has not yet been definitively established, it is now clear that terrestrial microorganisms can have sizes comparable to the ALH84001 forms, and therefore, the putative Martian microfossils cannot be arbitrarily dismissed solely on the basis of size. Knowledge of microbial life on the nanometer scale has been greatly extended and new information of great importance to astrobiology has been discovered concerning the limitations of cellular life on Earth. Knowledge concerning the upper size limit of prokaryotic life has also been increased by the discovery of a sulfide-metabolizing anaerobic bacterium. Thiomargarita namibiensis [9] is so large (cell size ~0.75 mm) that individual bacterial cells can be easily seen with the unaided eye.

1. Thermophiles and Psychrophiles as Analogs for Life on Mars and Europa It is now known that microbial extremophiles thrive in a wide range of environments on Earth. The discovery of these hardy life forms greatly enhances the possibility that viable microbiota might have existed in the ancient oceans or rivers of Mars or the oceans that exist today beneath the ice crust of Europa. Psychrophiles and thermophiles might also survive today, living within the hydrothermal vents, fumaroles, and deep crustal rocks of Mars. Psychrophiles may live or be cryopreserved in the ice crust of Europa or in the permafrost, glaciers, and polar ice caps of Mars. Sulfur- (S-) and sulfate-reducing bacteria and archaea are microbial extremophiles of significance to astrobiology. On Earth, they inhabit a wide variety of anaerobic and hypooxygenic eco-niches, such as geysers, volcanic fumaroles, deep-sea hydrothermal vents, deep crustal rocks, marine sediments, deep aquifers, animal intestines, soda lakes, high salinity lakes, soils, alkaline evaporates, and cryo-environments [10–12]. Sulfate or sulfur respiration is an anaerobic process with a combination of energy conservation by redox phosphorylation at the substrate level and electron flow on acceptors as sulfur or sulfur compounds. Hydrogen sulfide (H2S) is the end product of both catabolic processes (sulfur and sulfate respiration). Pikuta and Hoover [13] reviewed anaerobic sulfate- and sulfur-reducing bacteria on Earth and have suggested that they represent possible analogs for microbial life that might inhabit Jupiter’s volcanic moon, Io. This frozen world

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Figure 2. Viking 2 image of snow at the Lander site (48˚ N, 226˚ W) on May 18, 1979 (detector temperature: 18.1 ˚C) (Photo courtesy MSFC and NASA).

has active volcanoes driven by tidal heating from its proximity to the giant planet Jupiter. The temperature of Io ranges from –150 ˚C to over 2,000 ˚C. The surface of Io is covered with elemental sulfur and sulfur compounds, and the atmosphere of Io is primarily sulfur dioxide. Recent studies of sulfur- and sulfate-reducing bacteria at MSFC have resulted in the isolation and sequencing of two new species: (1) an alkaliphilic Sulfate-reducing bacterium from soda Mono Lake in northern California [14] (Desulfonatronum thiodismutans, sp. nov.) and (2) a thermophilic archaean (Thermococcus sulfurophilus, sp. nov.) [15] from the Rainbow deep-sea hydrothermal vent.

2. Sediments, Water, Snow, Glaciers, and Permafrost on Mars The carbonate minerals and magnetites in close association with possible microfossils in ALH84001 triggered intense debate concerning the possibility of life and water on Mars. The primary requirement for active microbial life on Earth is liquid water and a source of energy and organics, although some microbes can remain viable for long time periods in a frozen or desiccated state without water. Viking, Global Surveyor, and Odyssey images and data have provided dramatic evidence for water and ice on present-day Mars. The absence of water on Mars can no longer be thought to preclude the possibility of Martian microbial life or microfossils. Viking, Pathfinder, Global Surveyor, and Odyssey data have established that water was very abundant on ancient Mars and presently exists in the polar ice caps and permafrost of Mars. The Mars Global Surveyor Mars Orbiter Camera (MOC) images provide evidence that large quantities of liquid water were present on ancient Mars when the ALH84001 microfossils would have been formed. Viking images also provided dramatic evidence of water snow on Mars at the Lander site (48˚ N, 226˚ W) over several days in May of 1979 (Fig. 2). This is obviously snow and not frost as it is absent on vertical surfaces and collects in small depressions. The Viking detector temperature was – 8.10˚C, and thus it is impossible for this to be carbon dioxide (CO2) frost. The snow is on rocks in full sunlight, as indicated by the sharp spacecraft shadows. Solar heating of the soil and rocks on Mars should produce localized melting to permit liquid water to seep into the soil grain interstices and form thin water films within the permafrost. These films might be capable of supporting indigenous microbial life and the positive Viking Labeled Release data [16,17] should be carefully reexamined. Zuber et al. [18] analyzed elevation measurements from Mars Orbiter Laser Altimeter (MOLA) on Global Surveyor in 1998. These data show the volume of water ice in the Mars North Polar Cap is 1.2 million km3, about half the size of the Greenland Ice Cap. The Mars North Polar Cap in summer was 1,200-km across and 3.8-km thick with a shape showing it

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Figure 3. (a) MOC image of double rimed polygons in Mars permafrost and (b) double-rimmed polygons in permafrost of Kolyma lowlands of northeast Siberia. (Photos courtesy MSFC and NASA).

to be primarily composed of water ice. This is almost the same thickness as the Central Antarctic Ice Sheet at Vostok. Large areas of the ice sheet are extremely smooth—varying only a few feet over many miles, and other areas exhibit pinnacles and are cut by deep fracture crevasses and moulins (crevasses cut by flowing water) plunging to 1 km depth. The margins of the Mars polar cap are surrounded by giant conical mounds that are possibly pingos formed of ice and rocks tens of kilometers in diameter and over 1 km in height. There are also double-rimmed polygonal patterns in the permafrost similar to those known in patterned ground of the permafrost of Siberia, Alaska, and Antarctica. MOC, aboard the Mars Global Surveyor, also shows large amounts of water ice frozen in the Mars permafrost. MOC images show double-rimed polygons in the permafrost of Mars (Fig. 3 (a)) [20–24]. Images of similar double-walled polygons in permafrost were taken during the International Expedition Beringia by R. Hoover to the Kolyma lowlands of northeast Siberia (Fig. 3 (b)) and as also explained later in this volume by R. Paepe and Van Overloop, in Taylor Valley (Antarctica) in comparison with the Mars Moc image. The polar ice caps of Earth and Mars are paleomicrobiological traps capable of cryopreserving ancient microfossils, organic remains, and intact microbial cells in dead and viable states [19,25]. Prior meteorite impact events may have ejected crustal rocks and debris from sediments, volcanic deposits, glaciers, and permafrost into the atmosphere and onto the polar ice caps. Consequently, if microbial life presently exists or has existed on Mars in the geological past, the traces, remains, and biosignatures of this microbial life should be cryopreserved in a frozen state in the permafrost and polar ice caps. Marsic et al. [26–28] have described the DNA amplification and gene cloning of ribosomal RNA extracted from anaerobic psychrophiles of the Fox Tunnel of Alaska and from a living 40,000-yr-old Pleistocene moss cultured from samples collected in the Kolyma lowlands of northeastern Siberia. On Earth, the permafrost, ice wedges, glaciers, and polar ice sheets preserve organic chemicals, molecular biomarkers, intact cells, and viable ancient microorganisms, fungi, and mosses for several hundreds of thousands to millions of years, and analogous processes may operate on Mars. Abyzov et al. [29,30] detected viable Pleistocene microorganisms distributed throughout the Central Antarctic Ice sheet at Vostok, and Gilichinsky et al. [31,32] found ancient viable microorganisms cryopreserved in permafrost. The long-term preservation of microbes in ice is of astrobiological significance since many species of microorganisms can remain viable for geological periods of time frozen in glaciers, permafrost, and the polar ice caps of Earth. If life ever existed on these bodies, it might have remained viable, cryopreserved in the polar ice cap of Mars; the ice crusts of Europa, Ganymede, or Callisto; or the water ice of comets. Hoover et al. [33] discussed terrestrial ice-diatoms, snow algae, and cyanobacteria as analogs for the types of microbiota that might be capable of surviving in the ice of comets. Diatoms are the most prolific eukaryotic life forms of the terrestrial

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cryosphere. They are abundant in permafrost, glaciers, polar ice, and at the ice/ocean interfaces. Although diatoms are primarily photosynthetic organisms, some species live in the total darkness of deep-sea sediments and grow epiphytically on larger life forms in the hydrothermal vent ecosystem. Diatoms also employ heterotrophic nutritional modes to survive in the absolute darkness of the deep abyss or during the long polar winters. ALH84001 demonstrated that impact ejection phenomena can result in the transfer of crustal material from one planetary body to another. [34–36] Viable microorganisms exist in Antarctic ice, and complex microbial ecosystems thrive in deep crustal rocks and marine sediments. Rocks and ice ejected from Earth by large impact ejection events could transport terrestrial organic chemicals and microbiota into space, where they might contaminate comets, planets, or the parent bodies of carbonaceous chondrites. The Mars meteorites confirm that impact ejection can transport crustal rocks from Mars to Earth and that the terrestrial ecosystem is not closed. Carbonaceous chondrites can no longer be considered pristine because their parent bodies must have been contaminated by countless interactions and collisions with debris encountered during the past 4.6 Ga. Meteorites have obviously been extensively contaminated during their lifespan and exhibit dramatic heterogeneity the centimeter, millimeter, micrometer, and nanometer size scales. Any materials present on the meteorite when it entered the Earth’s atmosphere should be considered indigenous and only postarrival contaminants should be considered contamination. Furthermore, evidence for chemical and mineral biomarkers and microfossils that may be found in situ in meteorites should not be dismissed as contaminants solely because they may be similar to terrestrial microorganisms or biochemicals. The extreme hardiness of a wide variety of microbial extremophiles has clearly shown that the possibility of trans-planetary cross contamination of microbiota can no longer be totally excluded. Indeed, the ability of some microbes to survive phenomenal shocks, high pressure, hard vacuum, and deep-space temperatures for geological epochs combined with the presence on Earth of meteorites from Mars and the Moon indicate that microbial life may be far more widely distributed throughout the cosmos than previously thought possible.

3. Bioindicators and Biomarkers in Rocks and Meteorites The heated debate that followed the reported detection of biomarkers and possible microfossils in ALH84001 was reminiscent of the debate after the 1961 detection by Claus and Nagy [37,38] of organic biomarkers and possible microfossils in carbonaceous meteorites. Critics advanced a wide array of objections to the evidence for biomarkers and microfossils and the proponents ultimately retreated. Studies [39] established that forms such as Clause and Nagy had called organized elements are readily found in situ in freshly fractured surfaces of carbonaceous meteorites and cannot be dismissed as pollen contaminants. The other biomarkers that Claus and Nagy originally detected have also been confirmed. Extensive research on biomineralization, biological fractionation of stable isotopes, geomicrobiology, microbial extremophiles, and bacterial paleontology is now underway. [40] This debate has shown that it is critical that bioindicators and biomarkers be recognized and uniformly applied to terrestrial rocks, meteorites, and other astromaterials. Biomarkers that represent valid evidence of biogenic activity when found in terrestrial rocks should also be considered to represent valid evidence of biogenic activity, even if they are encountered in meteorites, astromaterials or returned samples from Mars, Europa, or comets. Since it is not possible to rule out prior planetary cross contamination by natural impact ejection phenomena, great care must be exercised (sterilization procedures, negative controls, in situ studies, etc.) to ensure that if returned samples contain Earth-like microorganisms they will not be automatically discarded as contaminants.

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There are a number of mineral and chemical bioindicators, e.g.: carbonates, silicates, phosphorites, polycyclic aramotic hydrocarbons (PAHs), hydrocarbons, and amino acids, that can also be produced by abiotic processes. It is now well known that microbial activity plays a critical role in the formation of the atmosphere and the mineral composition of the oceans. Photosynthesis by plants and marine phytoplankton govern the carbon (C):nitrogen (N):phosphorous (P) ratio in the deep oceans by the Redfield [41,42] ratio (C:N:P=106:16:1). This gives rise to important bioindicators that may be observed by gamma-ray or neutron spectroscopic detection of biologically significant element ratios. Individual bioindicators are not proof of biogenicity, but when found in association with other biomarkers the case becomes far more compelling. Important bioindicators and biomarkers include the following: • • •

• • •

• • • • • •

Biologically active elements: C, hydrogen (H), oxygen (O), N, P, S, silicon (Si), calcium (Ca), iron (Fe), magnesium (Mg), manganese (Mn), molybdenum (Mo), and copper (Cu). Ratios of bioelements: photosynthetic Redfield ratio—C:N:P=106:16:1. Biologically induced minerals: carbonates, tufa, ikaite, breunnerite, magnesite, siderite, calcite, aragonite, phosphorites, hydroxyl apatite, vivianite, pyrite, pyrrhotite, maghemite, mackinawite, hematite, goethite, magnetite, griegite, magnetosomes, framboidal iron and pyrite, millerite, todorokite, feitknechtite, argentite, silica biopolymers, and opal. Evaporites and clay minerals: dolomite, gypsum, halite, sulfates, illite, smectite, chlorite, and laterite. Chemical biomarkers and biomolecules: amino acids, chiral amino acids, fatty acids, lipids; nucleosides, nucleotide bases, guanylurea, urea, ammeline, melamine, purines, and pyrimidines. Geochemical fossils: PAHs, alkanes, isoalkanes cycloalkanes, humic acids, dichlorobenzene, thriophrenes, polymeric organic matter, cholestane, tetrapyrroles, porphyrins, asphaltene, lignins, kerogen, isoprenoids (pristine and phytane), steranes, triterpenoids, and methyl hopanes and hopanoids. Biological fractionation of stable isotopes: (δ13C; δ15N; δ18O; δ34S). Fossil structures: stromatolites, microbialites, oncolites, desert varnish, and banded iron formations. Microfossils and biogenic assemblages: microfossils of cells, cell walls, cysts, biofilms, magnetosomes in chain-of-pearls alignments, remains of cells, cell walls, flagella, processes, trichomes, and filaments and sheaths. Reproductive stages/life cycles: diplococci, chains of cells, hormogonia, spores, akinetes, heterocysts, and resting states. Microfossils of biologically consistent microbial ecosystems: lithified or mineralized microbial colonies and consortia. Ancient DNA and intact or viable microorganisms: cryopreserved in glaciers, ice sheets, and permafrost or desiccated and reserved in fossil tissues, amber, salt crystals, or other evaporite minerals.

Geomicrobiology is an important field of scientific research, and several important mineralogical biomarkers can be recognized. Many nanobacteria utilize phosphorus in the production of apatite shells, and many cyanobacteria produce phosphorite sheaths. Phosphorus and apatite are also present in carbonaceous chondrites. The recent discovery of extensive concentrations of microfossils of cyanobacteria and bacteria have provided convincing evidence of the biogenic origin of many of the phosphorite deposits on Earth, such as the great Khubsugul, Mongolia deposits. Chalk, limestone, and other carbonate rocks on Earth are produced by accumulations of the shells of microorganisms, such as foraminifera,

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coccoliths, discoliths, etc. The carbonate globules in SNC meteorites are important mineral biomarkers. The possible microfossils in ALH84001 were found in association with the carbonate globules. The carbonaceous chondrites include important carbonate minerals, such as Breunnerite ((Mg0.8Fe0.2)CO3), dolomite (Ca Mg(CO3)2), calcite (CaCO3), and magnesite (MgCO3). Dufresne and Anders [43] reported dolomite as small polycrystalline aggregates in the Orgueil meteorite and as well-rounded grains in Ivuna. They concluded that the dolomite crystal perfection and crystallization time implied a damp environment lasted for more than 1,000 yr on the parent body of the Orgueil meteorite. The Orgueil carbonates are of great interest because in 1963, Clayton [44] showed that the δ13Cratios in Orgueil lie in the 60‰ to 70‰ range. This clearly proves that the Orgueil carbonates are extraterrestrial since this value is significantly higher than ever seen in terrestrial carbonate rocks and biological materials. The δ13Cvalues for the meteoritic carbon are considerably higher than ever encountered on Earth. This fact clearly establishes that the carbon is indigenous and not the result of terrestrial contamination. The δ13Cvalues for meteorite organic matter are considerably lighter and constitute a valid biomarker that is consistent with biological fractionation of stable isotopes that are well known and accepted as indicating biogenic activity in terrestrial rocks. The dominant silica minerals in carbonaceous meteorites include olivine ((Mg,Fe)2SiO4), fosterite (MgSiO4) and fayalite (Fe2SiO4). Taylor et al. [45] studied the Murray and the Al Rais C2 carbonaceous meteorites and determined the δ18O values for olivine were always significantly lighter than the rock matrix values. This suggests that these components had dramatically different origins. Silicates and silica biopolymers are found in algae, e.g.: diatoms, chrysophytes, chrysomonads, and xanthophytes; sponge spicules; protozoans, e.g.: radiolarians, silicoflagellates, zoomastigophora, testacid sarcodina, siliceous foraminifera, and Rhizopod amebae; and in nanoplankton like loricate choanoflagellates. Indeed, the great diatomite deposits represent the most abundant form of common opal on our planet. Simpson and Volcani [46] have provided an excellent review of silicon and siliceous structures in biological systems. Claus and Nagy [37] reported the detection of some diatom frustules in the Orgueil meteorites, but they were dismissed as recent contaminants from terrestrial soil diatoms. Diatoms and other siliceous microbes produce instant microfossils that can remain intact and unaltered for hundreds of millions of years. The taxonomy of the diatoms, forams, etc. is based entirely on their shell morphology and their microstructure, which is completely adequate for their identification and classification to genus, species, and variety. Bacterial paleontology is essential to identify morphological biomarkers indicating biogenic activity in meteorites and astromaterials. 3.1. Chemical Biomarkers in Earth Rocks and Meteorites Earth rocks and meteorites contain important chemical fossils and biomarkers. The carbon content of the Orgueil meteorite was so high that it was at first thought to be from terrestrial contamination. The carbon in carbonaceous chondrites is predominantly a polymer-like material. Kerogenous organic compounds similar to peat, lignite coal, or tar are not soluble in common solvents. These forms of carbon are not known to be formed on Earth without the intervention of microbial processes and therefore are considered valid biomarkers. Carbonaceous chondrites also contain other biomarkers—complex organics including aliphatic and aromatic hydrocarbons, chiral amino acids (some with no known use in terrestrial biochemistry), purine and pyrimidine bases, fatty acids, lipids, porphyrins, isoprenoids, pristine, phytane, and hopanoids. Numerous independent investigators have studied this rich suite of complex organic chemicals indigenous to carbonaceous meteorites. Nooner and Oro [47] investigated extractable aliphatic hydrocarbons, and Olson et al. [48] studied the aromatic hydrocarbons in

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many different types of carbonaceous meteorites including Ivuna type CI1 (Ivuna, Alais, and Orgueil), Murray type CM2 (Murray, Mighei, Al Rais, Nogoya, Boriskino, Santa Cruz, Renazzo, Bells, Cold Bokkeveld), Ornans type CO3 (Ornans, Felix, and Lance) Karoonda type CK4 (Karoonda), and Vigarano type CV3 (Vigarano, Mokoia, and Warrenton). Olson et al. [48] reported detectable levels of aromatic hydrocarbons in the benzene eluates of the Murray meteorite, including naphthalene, 2-methyl naphthalene, biphenyl, acenaphthene, fluorine, phenanthrene, and a trace of anthracene. They also examined the aromatic hydrocarbons in the Bruderheim meteorite, the fossiliferous Precambrian gunflint chert and a hornblende diorite igneous rock and found that the aliphatic hydrocarbons of the meteorites had distribution patterns similar to those of gunflint chert. Subsequent studies have shown that carbonaceous chondrites contain a complex suite of chemical biomarkers, including polymeric matter and organics, complex cycloalkanes, purines, pyrimidines, amino acids, and even chiral amino acids [48–59]. The distribution of polycyclic aromatic hydrocarbons (m/e = 178 (phenanthrene (C14H10)), 202 (pyrene (C16H10)), 228 (chrysene (C18H12)), 252 (benzopyrene (C20H12)) in the Murchison meteorite [51] are very similar to the PAH distribution in ALH84001. In Murchison, Hayatsu et al. [52,53] detected indigenous purines and triazines, as well as 15 carboxylic acids and 11 aliphatic acids, which they could attribute to abiogenic processes, such as Fisher-Tropsch synthesis. Hydrocarbon analysis by gas chromatography/mass spectrometry was carried out on pristine samples of the Murchison meteorite collected immediately after its fall [54,55]. Kvenvolden et al. [56,57] detected 74 amino acids in Murchison, including a large number of non-protein species that are rare or completely unknown in terrestrial biology. They reported that the Murchison amino acids were racemic and had unusual stable isotope distributions [58,59], and therefore, were indigenous and could not have resulted from recent terrestrial contaminants. If the Murchison amino acids were recent contaminants, they should have not been racemic (equal mixtures of L- and D-enantiomers), rather they should have been almost exclusively the L-enantiomer. It is known that amino acids will become racemic over geological epochs—racemic mixtures are commonly found in ancient terrestrial organic matter. Engel and Nagy [60] recently detected a slight excess in L-amino acids in Murchison, indicating they were biogenic, i.e.: not Miller-Urey or Fisher-Tropsch synthesis products. The work of Engel et al. [61] and subsequently that of Cronin and Pizzarrello [62] has confirmed the presence of chiral amino acids indigenous to the Murchison meteorite. 3.2. Porphyrins in Earth Rocks and Meteorites Porphyrins are electron transport critical tetrapyrroles of profound importance to life on Earth. These complex biomolecules are encountered in life-critical pigments and enzymes. Magnesium is at the center of the tetrapyrrole ring in chlorophyll, which is one of several photosynthetic pigments that transduce light into chemical energy in plants, cyanobacteria, and other phototrophic microorganisms. Iron is at the center of the ring in the haeme groups of cytochromes responsible for transporting oxygen and carbon monoxide in blood and in the catalase enzyme, which catalyses the decomposition of cellular hydrogen peroxide. Porphyrin metal complexes are strong biomarkers, since porphyrins play a crucial role in the electron transport in oxidation-reduction reactions in almost all living organisms on Earth. The porphyrin ring is formed when four pyrrole rings (tetrapyrroles) condense with a metal ion (Fe, Mg, nickel (Ni), vanadium (V)) at the center of the porphin ring. Porphyrins are excellent biomarkers since they are both essential to critical biological processes and stable over geological time periods and conditions. As far back as 1935, Triebs [63] demonstrated that porphyrins are present in coal, phosphorites, oil shales, bituminous rocks, and petroleum. Park and Dunning [64] established by carbon isotope studies that the porphyrins

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were indigenous to petroleum. There are many pigments in living matter, e.g.: chlorophylls, bacteriochlorophylls, that are possible precursors for the petroleum porphyrins. Petroleum scientists have long considered the indigenous metallo-porphyrins as clear evidence of the biogenic origin of crude oil. Chlorins are porphin derivatives with hydrogen additions to the pyrrole ring, e.g.: dihydroporphin (chlorin) and tetrahydroporphin. Hodgson and Baker [65,66] investigated porphyrins in the Orgueil, Murray, Cold Bokkeveld and Mokoia carbonaceous chondrites and concluded that the meteorite porphyrins were indigenous and either from life forms different from terrestrial life or with a different diagenetic history after death. In Orgueil, they detected indigenous porphyrin pigments, which were spectrally similar to those in terrestrial sedimentary rocks. The absorption bands were consistent with vanadyl porphyrins in coal, petroleum, and oil shales. Vanadyl and nickel porphyrins are considered by petroleum geologists as some of the most important indicators of the biogenic origin of crude oil. These bands were not found in the solvent blank, granite, or ordinary chondrites. Hodgson and Baker [66] also detected substantial metal porphyrin complexes in Orgueil, Murray and Cold Bokkeveld, and Mokoia carbonaceous chondrites. They obtained excitation spectra with soret (390–413 nm) and nonsoret (490–615 nm) excitation bands present. Similar studies yielded negative results with other meteorites: Vigarano (C3), Indarch (Enstatite, E4), and the Bruderheim and Peace River stony chondrites (L6). The infrared (IR) spectra resemble those from organics in ancient terrestrial sedimentary rocks, e.g.: the Posidonia shale. Orgueil lacked chlorins (porphyrin derivatives where pyrrole rings have hydrogen additions). Since these closely related pigments are present in almost all terrestrial organisms, they should have been abundant if the meteorite porphyrins were due to recent terrestrial contaminants. (Chlorins very slowly convert to porphyrins and they are also absent in ancient terrestrial sediments.) Hodgson and Baker [66] have noted that indigenous porphyrins in Orgueil suggest the “strong possibility of biogenic agencies in the origin of the meteorite,” and the lack of chlorins indicates the indigenous meteoritic porphyrins are from prebiotic synthesis or ancient life. Nagy et al. [67] performed mass spectrometry analysis of Orgueil and found evidence of indigenous long-chain fatty acids. These organic chemicals showed patterns of molecular fragments (aliphatic and hydrocarbons) similar to fossil biological materials and petroleum. 3.3. Polymer-Type Organic Matter in Earth Rocks and Meteorites For many years, geochemical biomarkers have provided a standard tool for petroleum exploration. Good biomarkers must be stable for geologically significant periods of time (billions of years) and of definitive biogenic origin. Alteration of the original biochemicals by diagenesis and catagenesis is usually minimal and the basic carbon skeleton is preserved intact. Functional groups may be lost, e.g.: –OH, =O, etc., but the chemical structure derived from biological origins remains recognizable. Fossil biomolecules of cell membranes (fatty acids and lipids) are of known biological origin and are not produced abiotically. Fatty acids and long straight-chain hydrocarbon lipids are found in cell membranes of all three kingdoms of life on Earth. Nagy and Bitz [67] found fatty acids in cretaceous sedimentary rocks and meteorites. The long chain n-fatty acids they encountered in the Orgueil meteorite were absent in negative control blanks, indicating that they were not contaminants or introduced by their procedures. Murphy and Nagy [68] examined the sulfur compounds of the Orgueil lipid fraction. Hopanoids, isoprenoids, triterpanes, cholestanes, and steranes are important geochemical fossils and biomarkers because they are identifiable in the most ancient rocks and afford distinct biosignatures linked to specific kingdoms of life. Cholestane is the geologic product derived from the biochemical cholesterol and hopanoids are pentacyclic hydrocarbons

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Figure 4. (a) Diagenetic processes convert biologically produced cholesterol into geologic product 5 alpha(H) cholestane, (b) hopane, and (c) methylhopane and demethylaedhopane (25-norhopane) carbon skeletons.

that are derived from hopanes (Fig. 4). These types of biomarkers allow the petroleum geologists and astrobiologists to obtain information about the type of biological entity responsible for the geochemical, and therefore, they constitute important and valid biomarkers. Hopanoids are the predominant biosignatures of bacterial membranes, and they are totally unknown in archaea and rarely encountered in eukarya. In terrestrial sediments and rocks, there are 1014 tons of hopanoids derived from the membranes of ancient bacteria. This exceeds the total mass of carbon in all living organisms on Earth. The hopanoid carbon skeleton contains several chiral centers, so many stereoisomers are theoretically possible. The three different isomers found in the chiral centers at the C-17, C-21, and C-22 ring systems are the most significant in terrestrial rocks of the geosphere. In ancient marine sediments, Summons et al. [69] found 2-methylhopanes, which are derived from 2-Me-bacteriohopanepolyols (membrane lipids synthesized in large quantities only by cyanobacteria). Brocks et al. [70] extracted the cyanobacterial biosignatures (2methylhopanes) from 2.7 Ga old Archaean kerogenous shale. Astonishingly, C-28–C-30 steranes were also present in these rocks deep within Pilbara Craton of Australia. The detection of steranes in ancient shales dramatically extended the geological antiquity of eukaryotic biology. Steranes are valid biomarkers—biomolecules that are breakdown chemicals from complex sterols made only by eukaryotic life. These complex biomarkers show that the eukarye existed on Earth 500 Ma earlier than previously known. Although a few bacteria incorporate sterols into their membranes, none of the prokaryota form the elaborate sterols that are precursors for the C-28–C-30 steranes. Membranes in the cells of archaea are very different from those of the eukarya and none of the archaea has ever been found to synthesize sterols. Isoprenoids are branched-chain hydrocarbons with methyl substitutions in a pattern reflecting synthesis from one or more isoprene units. Geochemically, the most important isoprenoids are the saturated hydrocarbons phytane and pristine. Isoprenoids are biomarkers that are typically derived from photosynthetic microorganisms (with a possible contribution from isotopically light methanogenic archaea, which yield only small quantities of pristane and phytane relative to total biomass and no n-alkanes when pyrolyzed). Pristane is a common isoprenoid hydrocarbon, containing 19 carbon atoms, that is found in living organisms as well as in sediments and crude oils. Phytane is not found in living organisms. Pristane/phytane ratios <1 are associated with carbonate source rocks while values >4 are taken to indicate biological organic matter. Cronin and Pizzarello [71] found n-methyl and isoprenoid alkanes in Murchison using gas chromatography-mass spectroscopy, IR, and proton nuclear magnetic resonance spec-

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troscopy; however, they concluded that these valid biomarkers must have been due to terrestrial biological contamination. The aliphatic fraction of Murchison was found to be a structurally complex suite of branched alkyl-substituted, cycloalkanes (C-15–C-30). Gelpi and Oro [72] detected isoprenoids in 19 of the 20 carbonaceous chondrites they analyzed. They also concluded that these isoprenoids must have been the result of terrestrial biological contamination. Interpretation of these biomarkers as indigenous would have required a paradigm shift regarding biogenic activity and life in the meteorite parent body. When these petroleum biomarkers are found in terrestrial rocks they are readily accepted as the result of ancient biological activity. When similar suites of indigenous petroleum geochemicals are detected in meteorites they are dismissed as recent terrestrial contaminants or the result of abiogenic processes, e.g.: Miller-Urey or Fisher-Tropsch synthesis. Nagy [73] reviewed carbonaceous meteorites and the geochemistry of kerogens and hydrocarbons found in petroleum, coal, and oil shales. 3.4. The Biological Fractionation of Stable Isotopes The biological fractionation of the stable isotopes [74–76] of carbon, 13C and 12C, and sulfur, 34S and 32S, is a very well known and extremely important biomarker. Stable isotope studies and the detection of light carbon abundance are accepted as valid evidence of biogenic activity in extremely ancient Archaean terrestrial rocks that do not contain recognizable microfossils. Hence the observation of biological fraction of carbon in carbonaceous meteorites should also be considered strong evidence of indigenous biogenic activity in the parent body. Kvenvolden et al. [57] determined the carbon isotope abundances in the different carbonaceous phases of the Murchison meteorite and found the carbonate carbon to have a δ13C value of +45.4‰, which is vastly higher than terrestrial inorganic carbonates. In addition the organic carbon (Corg) of Murchison had a δ13C between –7.1‰ and –7.3‰. Terrestrial carbon of biological origin is significantly lighter (δ13C ranging from –10‰ to –60‰ depending on the nature of the organism and the carbon source. The δ13C values of the carbon in the Murchison mineral matrix and the soluble and insoluble polymeric carbon of Murchison are entirely consistent with biological fractionation of the Indigenous heavy carbon and imply biological activity on the meteorite parent body. The stable isotope results provide independent support of the evidence for indigenous microfossils and cyanobacterial ecosystems that have been detected in situ in freshly fractured samples of Murchison. As Nagy [73] concluded the carbon isotopes of the Murchison meteorite indicate that: the carbon is indigenous and not terrestrial; the δ13C of the Murchison Corg is dramatically lower than that of the mineral matrix; the δ13C of the Murchison Corg is higher than that of all terrestrial organic and inorganic matter; and biological fractionation is indicated in the meteorite stable carbon isotopes and it is clear that the terrestrial biological contamination is insignificant. Galimov [74] has investigated the thermodynamic isotopic fractionation of stable isotopes in a variety of biological systems. Figure 5 shows Galimov’s plots of the biological fractionation of stable carbon isotopes in the amino acids of several different life forms, such as (Fig. 5(a)) the green algae Chlorella pyrenoidosa, (Fig. 5(b)) the photosynthetic seaweed Gracilaria sp., and (Fig. 5(c)) the photosynthetic flagellated eukaryote Euglena gracilis. Galimov points out that the fractionation of the amino acids in the Murchison meteorite (Fig. 5(d)) is analogous to that seen in terrestrial biological systems. The values of δ13C for terrestrial abiotic carbon never exceeds, +10‰ and the stable isotope values of carbon in terrestrial life forms ranges from –4‰ (for autotrophs) to –85‰ (for methanotrophs). Since the stable isotope ratio δ13C for the carbon of Murchison meteorite ranges from +50‰ to +20‰, it is obviously impossible to interpret the Murchison amino acids as having resulted from contamination from any biological material found on Earth.

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Figure 5. Galimov data on the biological fractionation of stable carbon isotopes in the amino acids of (a) green algae Chlorella pyrenoidosa, (b) Gracilaria sp., (c) eukaryote Euglena gracilis, and (d) the Murchison CM2 carbonaceous meteorite (Courtesy E. Galimov).

Sulfate-reducing bacteria and archaea thrive in highly alkaline environments and in hot environments, such as geysers, fumaroles, and volcanic and deep-sea hydrothermal vents. The thermophilic and hyperthermophilic archaea represent the oldest known lineages of the sulfate-reducing bacteria on Earth. Some evidence indicates that these microorganisms have inhabited Earth for at least 3.5 Ga. The environments of early Earth, Mars, and Io may have been very similar, with water and intense volcanic activity. The sulfur- and sulfate-reducing microbes are excellent analogs for life on Mars and Io. Since dissimilatory bacterial sulfate reduction yields sulfides that are depleted in δ34S, the detection of biological fractionation as shown by δ34S values should be explored as a biomarker for optimizing the probability of finding evidence of life in Martian samples.

4. Morphological Biomarkers and Microfossils Morphological biomarkers include fossilized biofilms, desert varnish, microbialites, oncolites, laminated organo-sedimentary remains of bacterial and algal mats (stromatolites), nanofossils and microfossils of the carbonized or lithified remains of bacteria, archaea, cyanobacteria, algae, pollen, spores, resting stages, and organic-walled microfossils, such as hystrichospheres, pollen, and acritarchs. Research in bacterial paleontology [45] has made great progress in the recognition of fossil bacteria, algae, cyanobacteria, protozoans, fungi, actinomycetes, acritarchs, biofilms, and nanobacteria. Microfossils of cyanobacteria are well known from Cambrian and Precambrian cherts, oil shales, shungites, phosphorites and graphites [77–85]. Fossilized microbialites, and laminated organo-sedimentary structures (bacterial mats and stromatolites) were found in ~3.7 Ga old [86,87] rocks. Mojzsis [88] found molecular biomarkers in 3.8-Ga-old sedimentary rocks—the earliest trace

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of a biosphere. Rasmussen and Buick [89,90] found filamentous microfossils and petroleum in 3.2 Ga old volcanogenic massive sulfide deposits. Electron microscopy studies in the United States and Russia have revealed abundant lithified, carbonized, and embedded microfossils in every carbonaceous meteorite examined, but similar forms have been notably absent in other meteorites. These studies have concentrated on freshly fractured interior surfaces of the meteorites since the fusion crust and pre-existing cracks of meteorites can easily become contaminated by fungi, actinomycetes, and organotrophic bacteria. At the Paleontological Institute in Moscow, scanning electron microscope (SEM) studies were carried out on coated samples, and the x-ray analysis conducted with the LINK analyzer. At MSFC, uncoated samples were examined using ESEM and FESEM. These systems are capable of producing high resolution imaging of uncoated samples and biological materials and spectral analysis using energy dispersive x-ray spectroscopy (EDAX). Sterile sample handling techniques and optical microscopy methods have been used to examine numerous carbonaceous chondrites and stony meteorites. Field expeditions were carried out to investigate the morphology, life cycle processes, and ecological associations of living and cryopreserved bacteria, algae, and cyanobacteria in permafrost, cryoconite communities of Siberia and Alaska. Laboratory studies also included the Vostok deep ice cores [91–93], and magnetotactic bacteria and microfossils [94–98] in terrestrial rocks for comparison with lithified/carbonized remains found embedded in situ in a meteorite matrix.

5. Evidence of Magnetotactic Bacteria in Meteorites Magnetosomes and magnetite associated with magnetotactic bacteria are valid biomarkers. Anaerobic or microaerobic microorganisms produce magnetosomes with recognizable properties and definitive evidence of biogenicity. In 1975, Blakemore [99] announced the discovery of a magnetotactic bacterium, which he named Aquasprillum magnetotacticum, Schleiffer et al. [100] later transferred this species to the new genus, Magnetospirillum gen. nov., and described a new species, Magnetospirillum gryphiswaldense. Several other species of magnetotactic bacteria and algae have subsequently been found in anaerobic, microaerobic environments, and in soils, permafrost, and loess [101,102]. These microorganisms produce membrane-bounded magnetic crystals of magnetite (Fe3O4) or griegite (Fe3S4) [103–104]. The magnetite crystals are uniform and in the single-magnetic domain size range (typically about 35 to 150 nm) [105]. Matrix-controlled biomagnetite crystals are specific to species and occur in several configurations, e.g.: cubo-octahedral, elongated hexagonal prismatic, or bullet shaped. To optimize the magnetic properties, microorganisms usually configure the magnetites into one or more chains-of-pearls strands along the longitudinal axis of the organism [106,107]. Axis dipoles are oriented with the crystal axis—magnetite [108] or griegite [109] aligned to the chain direction. These microstructures are strong biomarkers because their unique morphological properties and chain-of-pearls distribution can be recognized in living organisms and rocks, and they distinguish biological magnetosomes from abiotic. Iron-reducing bacteria can also produce extracellular magnetite globules by dissimilatory iron reduction. The biomagnetite crystals produced in this way may exhibit lower crystallinity and a wider grain size than those found in magnetosomes. Mckay et al. [110] recently showed that the parallelepiped magnetites of ALH84001 exhibit the precise characteristics of biogenic magnetites. These results provide strong evidence for biogenic activity in this ancient Mars meteorite. Microfossils of magnetotactic bacteria with chains of magnetosomes and/or extracellular magnetites have now been detected in several meteorites, e.g.: ALH84001, Orgueil, Nogoya, and the Tagish Lake meteorites.

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Figure 6. (a) Orgueil microfossil with extracellular magnetite and chain-of-pearls magnetosomes, (b) magnetosomes in living purple sulfur bacteria Rhodopseudomonas rutilis, (c) ESEM image of microfossils in Nogoya carbonaceous meteorite and two-dimensional X-ray Maps in (d) Al, (e) Ca, (f) Fe, (g) O, and (h) S.

In 1967, Tan and VanLandingham [111] conducted transmission electron microscopy (TEM) studies of acid-resistant biological-like microstructures that they found in the Orgueil carbonaceous meteorite. They found numerous acid resistant cylindrical forms that were rounded on one end and tapered at the other (Fig. 6 (a)). TEM images show electrondense magnetites aligned as a chain of pearls along the longitudinal axis. Vainshtein [112,113] provided TEM images of living purple sulfur bacteria, Rhodopseudomonas rutilis, with similar configuration of magnetosomes (Fig. 6 (b)). An iron- and oxygen-rich microfossil in the Nogoya carbonaceous meteorite, which has similar microstructure to the magnetotactic microfossils of Orgueil, is shown in Fig. 6 (c) along with an accompanying ESEM image and two-dimensional x-ray maps showing the Al, Ca, Fe, O, and S distributions.

6. The Murchison Meteorite On the morning of September 28, 1969, a bright orange fireball with a silvery rim and a dull orange conical tail illuminated the sky over Victoria, Australia. Hundreds of black stones fell in a 1-mi wide and 10-mi long scatter ellipse at around the town of Murchison (36˚37’ S, 145˚14’ E). In December 2000, Hoover visited Murchison, Australia and discussed the event with several individuals who had witnessed the fireball and collected stones soon after their fall. Several reported hearing a hissing noise that sounded like “truck tires on a wet pavement” as soon as they saw the fireball. The fireball was seen to separate into several pieces, which was followed by the sound of several loud explosions. A strong smell of methyl alcohol was detected. Several of the Murchison stones landed on the golf course without scorching the grass or becoming embedded in the relatively soft ground.

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The low-density meteorite was obviously slowed and cooled by passage through denser parts of the atmosphere; one specimen penetrated a sheet metal roof of a shed and landed on hay without igniting the hay. Clearly, the Murchison stones hit the ground at terminal velocity and were not extremely hot when they arrived. Some Orgueil meteorite stones, which landed in France in 1864, were found with frost coatings shortly after their fall, indicating that the interior remained frozen and quickly cooled the fusion crust to allow moisture to condense and freeze. Lovering, who did the first scientific studies of Murchison, reported that frost was also observed on some nickel-iron meteorites.1 He received a sealed Murchison sample as he arrived at a television studio with Apollo 11 moon rocks one day after the fall. When the sealed Murchison bag was opened, a gas that had a strong odor of methyl alcohol was released. Pristine Murchison stones kept in sealed vials at the Victoria Museum still retain a strong sulfurous odor similar to asphalt and tar. Although the Murchison parent body remains unknown, the stable isotopes, and mineralogical analysis reveals that it certainly was not from Earth, the Moon, or Mars. Pollack et al. [114] note that the IR (0.4 to 1.1 δm)observations of Mars’ moon, Phobos, are similar to the spectral properties of the Murchison (CM2), Murray (CM2), and Orgueil (CI1) carbonaceous chondrites but different from basalt and other materials tested. They suggested that the 20-km diameter moon, Phobos, may be a carbonaceous chondrite that was captured by Mars in the early history of the solar system when Mars had a more extended gaseous envelope. The IR spectral reflectance properties of Murchison also resemble those of the 1,018-km diameter asteroid, Ceres [115]. Asteroids are considered the most probable parent bodies for the Ivuna-type (CI) and Mighei-type (CM) meteorites, but extinct cometary cores or protocometary bodies are also possibilities [116]. Observations of the Murchison fireball from the nearby towns of Mildura and Sheparton, Australia allowed Halliday and McIntosh [117] to compute an orbit for the parent body. Their calculations indicated a perihelion of 0.992 AU for an aphelion of 3 AU, which is consistent with the peak concentration of carbonaceous, i.e.: C-type, asteroids. This result implies that Murchison was overtaking Earth with a low relative velocity (~13 km/s) and that it would have never approached much closer to the Sun than the orbit of Earth. This result is consistent with the indigenous volatiles and suggests that conditions on the parent body may well have been conducive to microbiota, including photosynthetic bacteria and cyanobacteria that are known from cryoconite environments in glaciers and polar ice caps. During a portion of the orbit, Murchison would have been close enough to the Sun for indigenous water to have been in a liquid state, but not close enough for the volatiles to be driven off or for heat loads or radiation levels detrimental to microbial life. Seargent [118] noted the similarity of this orbit with periodic comet Finlay and the C-type Apollo asteroid 1979 VA (comet WilsonHarrington) and considered the possibility that Murchison may have come from a comet. The cosmic-ray exposure age (800,000 yr) [119] indicate that Murchison may have been a large boulder whose stem eroded from sustained cometary activity.

7. Microfossils of Cyanobacteria and Acritarchs in Carbonaceous Meteorites The search for microfossils in freshly fractured samples of carbonaceous meteorites has been carried out at MSFC using the Hitachi FESEM and the ElectroScan Corp. ESEM. Numerous samples from museums and meteorites collected during the Antarctica 2000 Expedition were studied. Mautner et al. [120] have shown that meteorite organic matter is a suitable nutrient for organotrophs and the meteorite fusion crust and old fractures are very susceptible to contamination by recent fungi, actinomycetes, and bacteria. During this research, fungal contamination of the fusion crust and pre-existent cracks, was detected in one sample of Murchison provided by the Field Museum in Chicago. These fungi were

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Figure 7. (a) Murchison meteorite microfossils similar to Nostocacean cyanobacteria tapered filament with apical cell and multiple cells in a common sheath, and (b) multiple filaments similar to Microcoleus cyanobacteria in common sheath in the Orgueil meteorite.

readily recognized as recent contaminants by several methods, such as the high oxygen and nitrogen content seen in the EDAX spectra, by the motion and behavior of the filaments under the electron beam, and by the appearance and color of these recent contaminants, which were clearly neither embedded nor lithified, as seen with optical microscope. Several pristine Murchison samples that had been carefully maintained in sealed vials since they were collected shortly after the meteorite landed in 1969 were provided on loan by Bill Birch of the Victoria Museum in Melbourne, Australia for this research. ESEM and FESEM studies of freshly fractured interior surfaces reveal that all of these meteorites contain abundant microfossils. Forms recognizable as the remains of biofilms, nanobacteria, cyanobacteria, and bacteria have been found. Figure 7 (a) shows a lithified form with a follicle-like structure (apical cell) at the apex (~2 δm in diameter) similar to known cyanobacteria of the genus Nostoc. These microstructures are virtually identical in size and morphology to the forms described as resembling filamentary blue-green algae (cyanobacteria) that were found in the Orgueil meteorite by Palik [121] of the Microbiological Institute of the Eötvös Lorand University in Budapest. This form is in proximity to three sheath covered cells and multiple filaments within a common sheath, similar to microfossils of cyanobacteria (cf. Phormidium sp.and Microcoleus sp.) that are preserved in the Cambrian phosphorites of Khubsugul, Mongolia. In Fig. 7.b. multiple trichomes in a common sheath are foundt in situ in the Orgueil meteorite. These forms are similar to those known in both living halophilic cyanobacteria Microcoleus spp. and fossil forms that are known from the Cambrian phosphorites of Khubsughul, Mongolia. In Fig. 7 (b), it is seen that another group of trichomes is only partially exposed, with the rest of the sheath projecting downward and encased in the mineral matrix of the meteorite. Clusters of coccoidal bacteria are seen on the surface of the horizontal group of sheaths. Figure 8 shows a long hollow sheath, similar to that of Nostocacean cyanobacteria, surrounded by embedded remains of coiled hormogonia in the Murchison meteorite. Since cyanobacteria are photosynthetic microorganisms, they are not logical candidates for recent contaminants because they would not have reason to invade the interior of the black meteorite stones. Acid-resistant organic-walled microfossils and acritarchs have been found in several meteorites. Claus and Nagy first described them, and subsequently, they have been extensively studied [122–130]. Rossignol-Strick and Barghorn [39] concluded that these acidresistant, hollow-walled forms were definitively not pollen. They also considered them to be indigenous to the Orgueil meteorite and of extraterrestrial origin. Timofejev [131] photographed (Fig. 9 (a)) numerous acritarch-like microfossils found in the Mighei meteorite. Figure 9 (b) and (c) show two of the acritarch-like microfossils found in the Orgueil and Murchison meteorites.

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Figure 8. Embedded remains in the Murchison meteorite showing emergent trichomes, sheath, and coiled hormogonia of cyanobacteria.

Figure 9. (a) Acritarch-like microfossils found in the Mighei meteorite by Timofejev and ESEM images of Acritarch-like forms found by Hoover in (b) Mighei meteorite, and (c) in a pristine Murchison sample collected near Murchison East, Victoria (donated by John Lovering to the Victoria Museum on Feb. 10, 1971).

Since acritarchs are extinct microorganisms of uncertain affinities (probably resting spores of extinct marine phytoplankton), they cannot be considered as logical suspects for recent contaminants for these carbonaceous meteorites.

8. Conclusions Carbonaceous meteorites contain a complex suite of chemical, mineral, and morphological biomarkers. Independent and later collaborative investigations at NASA’s MSFC and the PIN/RAS have resulted in the detection of a suite of large, clearly biogenic, lithified, and embedded microstructures that are interpreted to be indigenous microfossils. Many of the forms found are similar to known photosynthetic microbes or extinct algae. In some cases, they have been found in complex assemblages of consistent microbial ecosystems and consortia. They are commonly encountered embedded and carbonized or lithified in recently fractured surfaces of the meteorite matrix. Using these methodologies, a single recognizable pollen grain has yet to be encountered, and based on their microbiology and the type of preservation, these microfossils that have been found cannot be dismissed as recent pollen contaminants. Many are recognizable as bacteria, cyanobacteria, algae, and acritarchs. Microfossils have been encountered in every carbonaceous chondrite studied: CI (Alais, Tagish Lake, and Orgueil), CM (Murchison, Mighei, Murray, and Nogoya), CO (Rainbow, Kainsaz; DaG 749), CV (Allende and Efremovka), CR (Acfer324), and CK (Karoonda), belonging to the petrographic types 1, 2, 3, 5, and 7. Similar microstructures were not found in the non-carbonaceous meteorites that were studied, including a diogenite (DIO) from

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Tunisia (Tatahouhine, DIO); several ordinary chondrites, e.g.: Holbrook, L/LL6; Nikolskoye, L4; Barratta, L4; and stony meteorites collected on the Moulton escarpment of the Thiel Mountains (TIL99001–TIL99019) during the Antarctica 2000 Expedition. 8.1. Evidence of Indigenicity Microfossils have been found embedded in freshly fractured surfaces of the meteorite matrix and elemental distributions by EDAX analysis (C, O, Fe, Ni, S, N, and P) and two dimensional x-ray maps indicate that many of the microfossils are lithified and/or carbonized. Consequently, they cannot be interpreted as recent contaminants and are interpreted as indigenous. Some have affinities to extinct groups—acritarchs and hystricospheres—which would not be expected to contaminate meteorites that were observed to fall within the last century. 8.2. Evidence for Biogenicity Some of the forms have recognizable cell walls, membranes, sheaths, and glycocalyx. Many are present as colonies, coccoidal clusters, and macrocolonies (similar to cyanobacteria and purple sulfur bacteria). Evidence of life cycle processes—including replication, e.g.: dividing cells/diplococci, hormogonia, spores, and chains of cells—as well as ecologically consistent microbial assemblages and communities (similar to cryoconite communities from Antarctica, including Microcoleus spp., Phormidium frigidum, and Nostoc spp.) has been encountered. Many of the microfossils that were found exhibit strong similarities to living cyanobacteria, magnetotactic bacteria, living algae, and extinct plankton. On one sample of the Murchison meteorite, on the fusion crust and in old fissures, there was evidence of recent fungi and actinomycetes that are interpreted as recent (postarrival) biocontaminants. Microbiota or microfossils that may have been present on the meteorite when it entered Earth’s atmosphere, should be considered indigenous. Therefore, this suite of complex microstructures found in situ in freshly fractured surfaces of carbonaceous meteorites is interpreted as representing the indigenous biogenic remains of microbiota and microbial communities that were present on the meteorite parent body prior to arrival at Earth’s surface.

Acknowledgments Great thanks go to Alexei Yu. Rozanov for extensive collaborations, Greg Jerman and James Costen for electron microscopy support, Bill Birch, Director of the Victoria Museum in Melbourne for pristine samples of the Murchison meteorite.

Endnote 1.

Private communication between John Lovering and Richard Hoover. December 2000.

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[26] Marsic D, Pikuta EV, Hoover RB, Ng JD. Cloning of the 16S ribosomal RNA gene of a psychrophilic bacterium from the Alaskan fox Permafrost Tunnel. In: Hoover RB, editor. Instruments, methods, & missions for astrobiology, IV. Proc. SPIE 2001; 4495: 313–24. [27] Marsic D, Hoover RB, Gilinchinsky DA, Ng JD. Gene cloning of the 18S rRNA for ancient viable moss from the permafrost of northeastern Siberia. In: Hoover RB, editor. Instruments, methods, & missions for astrobiology, II. Proc. SPIE 2000; 3755: 163–73. [28] Marsic D, Hoover RB, Gilichinsky D, Ng JD. Extraction and amplification of DNA from an ancient moss.://www.promega.com/enotes/applications/ap0004_print.htm. Promega eNotes; 1999. Last accessed November 10, 2003. [29] Abyzov SS. Microorganisms in the Antarctic ice. In: Friedman EI, editor. Antarctic Microbiology. New York: Willey-Liss, Inc.; 1993. 265–96 p. [30] Abyzov SS, Mitskevitch IN, Puglozova MN, Barkov NI, Lipenkov VYa, Bobin NE, Koudryashov BB, Pashkevich VM. Long-term conservation of viable microorganisms in ice sheet of Central Antarctica. In: Hoover RB, editor. Instruments, methods, & missions for astrobiology. Proc. SPIE 1998; 3441: 75– 84. [31] Gilichinsky D, Wegener S, Vishnivetskaya T. Permafrost microbiology. Permafrost and Periglacial Proc. 1995; 2: 281–91. [32] Gilichinsky DA. Permafrost as a microbial habitat: extreme for the Earth, favorable in space. In: Hoover RB, editor. Instruments, methods, & missions for astrobiology. Proc. SPIE 1997; 3111: 472–80 [33] Hoover RB, Hoyle F, Wickramasinghe NC, Hoover MJ, Al-Mufti S. Diatoms on Earth, comets, Europa and in interstellar space. Earth, Moon, and Planets1986; 35: 19–45. [34] O’Keefe JD, Ahrens TJ. Meteorite impact ejecta: dependence of mass and energy lost on planetary escape velocity. Science 1977; 198: 1248–51. [35] Melosh HJ. Ejection of rock fragments from planetary bodies. Geology 1985; 13: 144–8; The rocky road to panspermia. Nature 1988; 332: 687–8; Impact ejection, spallation and the origin of meteorites. Icarus 1984; 56: 260–99. [36] Gladman BJ, Burns JA. Mars meteorite transfer: simulation. Science 1996; 274: 161–2. [37] Claus G, Nagy B. A microbiological examination of carbonaceous chondrites. Nature 1961; 192: 594– 6. [38] Nagy B, Meinschein WG, Hennessy DJ. Mass spectroscopic analysis of the Orgueil meteorite: evidence for biogenic hydrocarbons. Ann. N. Y. Acad. Sci. 1961; 93: 25–35. [39] Rossignol-Strick M, Barghoorn ES. Extraterrestrial abiogenic organization of organic matter: the hollow spheres of the Orgueil meteorite. Space Life Sci. 1971; 3: 89–107. [40] Rozanov AYu, Zavarzin GA. Bacterial paleontology. In: Hoover RB, editor. Instruments, methods, & missions for astrobiology, Proc. SPIE 1998; 3441: 218–84. [41] Redfield AC. On the proportions of organic derivations in sea water and their relation to the composition of plankton. In: James Johnston Memorial Volume. Liverpool; 1934. 176–92 p. [42] Redfield AC. The biological control of the chemical factors in the environment. Amer. Sci. 1958; 46: 225–21. [43] DuFresne ER, Anders E. On the chemical evolution of carbonaceous chondrites. Geochim. Cosmochim. Acta 1962; 26: 1085–114. [44] Clayton RN. Carbon isotope abundance in meteorite carbonates. Science 1963; 140: 192–3. [45] Taylor Jr. HP, Duke MB, Silver LT, Epstein S. Oxygen isotope studies of minerals in stony meteorites. Geochim. Cosmochim. Acta 1965; 29: 489–512. [46] Simpson TL, Volcani BE, editors. Silicon and siliceous structures in biological systems. New York: Springer-Verlag; 1981. 1–585 p. [47] Nooner DW, Oro J. Organic compounds in meteorites, 1. Aliphatic hydrocarbons. Geochim. Cosmochim. Acta 1967; 31: 1359–94. [48] Olson RJ, Oro J, Zlatkis A. Organic compounds in meteorites, 2. Aromatic hydrocarbons. Geochim. Cosmochim. Acta 1967; 31: 1935–48. [49] Folsomme CE, Lawless J, Romiez M, Ponnamperuma C. Heterocyclic compounds indigenous to the Murchison meteorite. Nature 1971; 232: 108–9. [50] Kvenvolden KA, Lawless JG, Pering K, Peterson E, Flores J, Ponnamperuma C, Kaplan IR, Moore C. Evidence for extraterrestrial amino acids and hydrocarbons in the Murchison meteorite. Nature 1970; 228: 923–6. [51] Basile BP, Middleditch BS, Oro J. Polycyclic aromatic hydrocarbons in the Murchison meteorite. Organic Geochem. 1984; 5: 211–6. [52] Hayatsu R, Studier MH, Moore LP, Anders E. Purines and Triazines in the Murchison meteorite. Geochim. Cosmochim. Acta 1975; 39: 471–88. [53] Hayatsu R, Matsuoka S, Scott RG, Studier MH, Anders E. Origin of organic matter in the early solar system-VII. The organic polymer in carbonaceous chondrites. Geochim. Cosmochim. Acta 1977; 41: 1325–39.

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[83] Zhegallo EA, Rozanov AYu, Ushatinskaya GT, Hoover RB, Gerasimenko LM, Ragozina AL. Atlas of microorganisms from ancient phosphorites of Khubsughul (Mongolia). NASA/TP—2000–209901. Marshall Space Flight Center: MSFC, AL; 2000. 1–167 p. [84] McKay DS, Rozanov AYu, Hoover RB, Westall F. Phosphate biomineralization of Cambrian microorganisms. Proc. SPIE 1998; 3441: 170–6. [85] Rozanov AYu, Zhegallo EA, Hoover RB. Microbiota of the Botogol Graphites. In: Hoover RB, editor. Instruments, methods, & missions for astrobiology II. Proc. SPIE 1999; 3775: 38–48. [86] Schopf JW, editor. Earthís earliest biosphere: its origin and evolution. Princeton: Princeton University Press; 1983. 1–543 p. [87] Grotzinger JP, Knoll AH. Stromatolites in Precambrian carbonates: evolutionary mileposts or environmental dipsticks? Ann. Rev. Earth and Planet. Sci. 1999; 27: 313–58. [88] Mojzsis, SJ, Harrison TM. Vestiges of a beginning: clues to the emergent biosphere recorded in the oldest known sedimentary rocks. GSA Today 2000; 10: 1–2. [89] Rasmussen B. Filamentous microfossils in a 3,225 million-year-old volcanogenic massive sulfide deposit. Nature 2000; 405: 676–9. [90] Rasmussen B, Buick R. Oily old ores: evidence for hydrothermal petroleum generation in an Archean volcanogenic massive sulfide deposit. Geology 2000; 28: 731–4. [91] Marsic D, Hoover RB, Gilichinsky DA, Ng JD. Gene cloning of the 19s rRNA of an ancient viable moss from the permafrost of northeastern Siberia. In: Hoover RB, editor. Instruments, methods, & missions for astrobiology II, Proc. SPIE 1999; 3775: 163–75. [92] Abyzov SS, Mitskevitch IN, Paglazova MN, Hoover RB, Ivanov MV. Microorganisms and unicellular algae in the Ice Sheet of Antarctica. In: Hoover RB, editor. Instruments, methods, & missions for astrobiology II, Proc. SPIE 1999; 3775: 176–87. [93] Hoover RB, Abyzov SS, Ivanov MV. Environmental scanning electron microscopy investigations of ancient microorganisms from deep ice above Lake Vostok. In: Hoover RB, editor. Instruments, methods, & missions for astrobiology II, Proc. SPIE 1999; 3775: 187–98. [94] Zhmur SI, Rozanov AYu, Gorlenko VM. Lithified remnants of microorganisms in carbonaceous chondrites. Geochem. Int. 1997; 35: 58–60. [95] Hoover RB. Meteorites, microfossils, and exobiology. In: Hoover RB, editor. Instruments, methods, & missions for the investigation of extraterrestrial microorganisms. Proc. SPIE 1997; 3111: 115–36. [96] Hoover RB, Rozanov AYu, Zhmur SI, Gorlenko VM. Further evidence of microfossils in carbonaceous chondrites. In: Hoover RB, editor. Instruments, methods, & missions for astrobiology. Proc. SPIE 1998; 3441: 203–16. [97] Gerasimenko LM, Hoover RB, Rozanov AYu, Zhegallo EA, Zhmur SI. Bacterial paleontology and studies of carbonaceous chondrites. Paleontological J. 1999; 33: 439–59. [98] Hoover RB, Rozanov AYu. Biomorphic microstructures in Mighei carbonaceous meteorite. In: Hoover RB, editor. Instruments, methods, & missions for astrobiology II, Proc. SPIE 1999; 3775: 120–30. [99] Blakemore R. Magnetotactic Bacteria. Sci. 1975; 190: 377–9. [100] Schleiffer K-H, Schuler D, Spring S, Weizenegger M, Amann R, Ludwig W, Kohler M. The genus Magnetospirillum gen. nov., description of Magnetospirillum gryphiswaldense sp. nov. and transfer of Aquaspirillum magnetotacticum to Magnetospirillum magnetotacticum. Syst. appl. Microbiol. 1991; 14: 379–85. [101] Fassbinder JWE, Stanjek H, Vali H. Occurrence of magnetic bacteria in soil. Nature 1990; 343: 161–3. [102] Maher B, Thompson R. Paleoclimatic significance of the mineral magnetic record of the Chinese loess and paleosols, Quater. Res. 1992; 37: 155–70. [103] Heywood BR, Bazylinski DA, Garratt-Reed A, Mann S, Frankel RB. Controlled biosynthesis of greigite (Fe3S4) in magnetotactic bacteria, Naturwissenschaften 1990; 77: 536–8. [104] Heywood BR, Mann S, Frankel RB. Structure, morphology and growth of biogenic greigite (Fe 3S4). In: Alpert M, Calvert P, Frankel RB, Rieke P, Tirrell D, editors. Materials synthesis based on biological processes. Pittsburgh: Materials Research Society; 1991. 93–108 p. [105] Bazylinski DA, Frankel RB, Heywood BR, Mann S, King JW, Donaghay PL, Hanson AK. Controlled biomineralization of magnetite (Fe3O4) and greigite (Fe3S4) in a magnetotactic bacterium. App. and Environ. Microbiol. 1995; 61: 3232–9. [106] Bazylinski DA, Heywood B, Mann S, Frankel RB. Fe3O4 and Fe3S4 in a bacterium. Nature 1993; 366: 218. [107] Bazylinski DA. Anaerobic production of single-domain magnetite by the marine, magnetotactic bacterium, strain MV–1. In: Frankel RB, Blakemore RP, editors. Iron biominerals, New York: Plenum; 1990. 69–77 p. [108] Bazylinski DA, Garratt-Reed AJ, Frankel RB. Electron microscopic studies of magnetosomes in magnetotactic bacteria, Microscopy Res. Techn. 1994; 27: 389–401.

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Survival of Microorganisms in Space, an Experimental Contribution to the Discussion on Viable Transfer of Life in the Solar System Gerda HORNECK German Aerospace Center DLR, Institute of Aerospace Medicine, 51170 Cologne, Germany Abstract. The concept of interplanetary transfer of life requires that organisms cope with three major challenges: (1) The escape process, (2) the long-term stay in space, and (3) the landing process. The first step involves hypervelocity impact by comets or asteroids under strong or moderate shock metamorphism of the ejected microbebearing rock fragment. Experiments have shown that bacterial spores can survive such a simulated meteorite impact. The second step deals with the ability of microorganisms to withstand the complex interplay of the parameters of space, e.g.: vacuum, ultraviolet and ionizing radiation, and temperature extremes, when traveling in space over extended periods of time. Experiments in space, such as on board of Apollo, Spacelab 1 (SL 1), the Long Duration Exposure Facility (LDEF), FOTON, MIR, and the European Retrievable Carrier (EURECA), as well as at space simulation facilities on ground, have given the following five results: (1) Extraterrestrial solar UV radiation is a thousand times more efficient than UV at the surface of the Earth and kills 99% of bacterial spores within a few seconds; (2) space vacuum increases the UV sensitivity of the spores; (3) although spores survive extended periods of time in space vacuum (up to 6 yr) genetic changes occur, such as increased mutation rates; (4) after 6 yr in space, up to 70% of bacterial spores survived if protected against solar UV radiation and dehydration; (5) spores could escape a hit of a cosmic HZE particle, e.g.: iron ion, for up to 1 Ma. Calculations using radiative transfer models for cosmic rays and biological data from accelerator experiments have shown that a meteorite layer of 1 m or more effectively protects bacterial spores against galactic cosmic radiation for 1 Ma or more. It is concluded that radiation-resistant microbes could survive a journey from one planet to another in our solar system if they are located inside a meteorite thus shielded against cosmic radiation. However, viable transport between solar systems seems to be not possible, assuming impact ejection as the first step. The last step, capture and landing on a planet depends very much on the atmospheric conditions and the size of the meteorite. So far, few experiments have been done to investigate the effects of the landing process.

Introduction A century ago, S. Arrhenius formulated the theory of Panspermia, which postulates that microscopic forms of life, e.g.: spores, can be propagated in space and driven by the radiation pressure of the sun as a mechanism of transport for the germs of life from one planet to another [1]. Recent discoveries, such as the Martian meteorites, the high UV resistance of mi-

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Figure 1. Steps of a hypothetical scenario of interplanetary transfer of life using meteorites as transport vehicle [3].

croorganisms at the low temperature of deep space, and the recovery of viable spores after extended periods of time in space [2], have given support to revisit the theory of Panspermia. During a hypothetical interplanetary transfer process, the organisms have to cope with the following three major challenges: (1) The escape process, i.e.: removal to space of biological material that has survived being lifted from the surface to high altitudes; (2) the interim state in space, i.e.: survival of the biological material over time scales comparable with the interplanetary or interstellar passage; and (3) the entry process, i.e.: the nondestructive deposition of the biological material on another planet (Fig. 1). In the following, results from experimentation in space will be presented to test the feasibility of step two, i.e.: the impact of the space environment on the seeding of life throughout the solar system.

1. Bacterial Endospores as Test Organisms Many microorganisms found in terrestrial soils are capable of forming spores to cope with unfavorable environmental conditions; particularly, bacterial endospores withstand extremely hostile conditions in the dormant state. They exhibit a high degree of resistance to inactivation by various physical and chemical stresses, such as desiccation, extreme temperatures, UV and ionizing radiation, and various aggressive chemical insults including alcohol, acid and basic solutions, and oxidizing agents. Hence, bacterial endospores have been recognized as the hardiest known forms of life on Earth [4]. The high resistance of Bacillus (B.) endospores is mainly due to two factors: (1) A dehydrated, highly mineralized core enclosed in a thick protective envelop, the cortex, and the spore coat layers (Fig. 2), and (2) the saturation of their DNA with small, acid-soluble proteins whose binding greatly alters the chemical and enzymatic reactivity of the DNA [5]. In the presence of appropriate nutrients, spores respond rapidly by germination and outgrowth, resuming vegetative growth and cell replication. Hence, spore formation represents a strategy by which a bacterium escapes temporally and/or spatially from unfavorable conditions; bacterial endospores exhibit incredible longevity—survival times of 25 to 250 Ma have been reported [6,7]. Because of their microscopic size, they can be easily relocated, e.g.: by wind and water, over long distances to remote areas.

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Figure 2. Electronmicrograph of a spore of B. subtilis with the inner core containing the DNA surrounded by protective layers, the long axis of the spore is 1.2 μm, the core area 0.25 μm2 (courtesy of S. Pankratz).

Their exceptionally high resistance against environmental extremes over long periods of time makes bacterial endospores suitable candidates for studying the likelihood of transport of life between the planets of our solar system. During such a hypothetical interplanetary transfer, the spores would be exposed to a complex interplay of environmental stresses, such as shock waves and high temperatures during the ejection process [8], extreme vacuum, intense radiation from the sun and of galactic origin, and varying temperatures depending on the orientation to the sun during the interim stay in outer space [9], and finally, accelerations and high temperatures during the entry into a planetary atmosphere and landing on the planet’s surface. The responses of B. subtilis spores to these different parameters of a hypothetical trip between the planets have been studied in ground-based spacesimulation facilities and in several space experiments. The results are summarized in Sections 2–4.

2. Escape From a Planet Hypervelocity impacts of large objects, such as meteorites, asteroids, or comets, are considered to be the most plausible process capable of ejecting microbe-bearing surface material from a planet or moon into space. The peak shock pressure received by the Martian meteorites, so far detected on Earth, range from about 20 GPa to about 45 GPa with estimated post-shock temperatures between about 100 ˚C at 20 GPa and about 600 ˚C at 45 GPa. Although these impacts are very energetic, a certain fraction of ejecta is not heated above 100 ˚C. These low-temperature fragments are ejected from the so-called spall zone, i.e.: the surface layer of the target, where the resulting shock is considerably reduced by superimposition of the reflected shock wave on the direct one [10,11]. It has been calculated that within the last 4 Ga more than 109 fragments with a diameter of ≥2 m and temperatures ≤100 ˚C were ejected from Mars, of which about 5% arrived on Earth after a journey in space of ≤8 Ma. The corresponding numbers for a transfer from Earth to Mars are about 108 fragments ejected from the Earth with about 0.1% arriving on Mars within 8 Ma [9]. During the preceding period of heavy bombardment, even 10 times that amount is estimated. Hence, the Martian meteorites, so far detected on Earth, probably represent only a diminishing fraction of those imported from Mars within Earth’s history.

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Table 1. Parameters of outer space [13].

In experiments, simulating impacts comparable to those experienced by the Martian meteorites, the survival of microbes was tested after subjecting spores of B. subtilis to accelerations, jerks, or shock waves [12]. In shock recovery experiments with an explosive set-up, the survival of spores of B. subtilis was studied using a shock treatment in the pressure range that some Martian meteorites have experienced [8]. It was found that a substantial fraction of spores (up to 10–4) were able to survive a peak shock pressure of 32±1 GPa and a post-shock temperature of about 250 ˚C. These data support the hypothesis that bacterial spores may survive an impact-induced escape process in a scenario of interplanetary transfer of life. Assuming a mean spore density of 108 spores/g in, for example, desert soil or rock, a 1-kg rock would accommodate ~1011 spores, of which up to 107 could survive even extremely high shock pressures that occur during a meteorite impact. At more moderate shock waves as they would occur in the spall zone of an impact, even substantially higher survival rates are expected.

3. Responses of Microorganisms to the Environment of Outer Space 3.1. Parameters of Outer Space That Are a Potential Threat to Microbial Life The environment that microorganisms have to cope with in outer space is characterized by a high vacuum, an intense radiation climate of galactic and solar origin, and extreme temperatures (Table 1). In free interplanetary space, pressures down to 10–14 Pa prevail. Within the vicinity of a body, the pressure may significantly increase due to outgassing. In a low Earth orbit of an altitude below 500 km, pressure reaches 10–7–10–4 Pa. The major constituents of this environment are molecular oxygen and nitrogen as well as highly reactive oxygen and nitrogen atoms. In the vicinity of a spacecraft, the pressure further increases, depending on the de-

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gree of outgassing of the spacecraft itself. In the Shuttle cargo bay, a pressure of 3×10–5 Pa was measured. The planets in this solar system are continuously bombarded by charged particles coming from unknown sources outside our solar system and from the sun. The galactic cosmic rays are composed of energetic particles, which cover a broad spectrum of energy and mass values; ~98% are atomic nuclei and 2% are electrons and positrons. The nuclear component consists of ~87% protons, about 12% α particles, and ~1% nuclei of Z>2, the so-called HZE particles. These nuclei are stripped of all their orbital electrons and have traveled for several million years through the galaxy before entering the solar system. When these charged particles enter the solar system, they interact with the outbound streaming of the solar wind and the interplanetary magnetic field, which vary with the solar activity. In interplanetary space, the annual radiation dose amounts to ≤0.1 Gy/a, depending on mass shielding with the highest dose at 0.15 g/cm2 shielding due to built up radiation [14]. The spectrum of solar electromagnetic radiation spans over several orders of magnitude, from short-wavelength x-rays to radio frequencies. At the distance of 1 AU (Sun to Earth), solar irradiance amounts to 1,360 W m–2, which is the solar constant. Of this radiation, 45% is attributed to the infrared fraction, 48% to the visible fraction, and only 7% to the ultraviolet fraction. The extraterrestrial solar spectral UV irradiance has been measured during several space missions, such as SL 1 and EURECA [15]. The temperature of a body in space depends on its position regarding the Sun, and also on its surface, size, and mass. It is determined by the absorption and emission of energy. In Earth orbit, the energy sources are the solar radiation (1,360 W m–2), the Earth albedo (480 W m–2), and terrestrial radiation (230 W m–2). In Earth orbit, the temperature of a body can reach extreme values. In different space exposure experiments, the samples were subjected to temperatures in the range of 243–318 K [3,16]. The time it would take for boulder-sized rocks to travel from one planet of our solar system to another, e.g.: from Mars to Earth, by random motion has been calculated to range between several hundred thousand to millions of years [17]; however, smaller, e.g.: microscopic, particles that are more frequent might only need a few years. For an interstellar transport, such as from one solar system to another, even longer time periods, up to 10 Ma may be required [3]. 3.2. Effects of Space Vacuum Vacuum leads to extreme desiccation of the cells exposed to it. This desiccation may cause dramatic changes in such important biomolecules as lipids, carbohydrates, proteins, and nucleic acids. On desiccation, the lipid membranes of cells undergo dramatic phase changes from planar bilayers to cylindrical bilayers [18]. The carbohydrates, proteins, and nucleic acids undergo so-called Maillard reactions, i.e.: amino-carbonyl reactions, to give products that become cross linked, thus, eventually leading to irreversible polymerization of the biomolecules [18]. Concomitant with these structural changes are functional changes, including altered selective membrane permeability, inhibited or altered enzyme activity, decreased energy production, alteration of genetic information, etc. Damage to the DNA, like increased mutation rates and DNA strand breaks were observed in bacterial spores recovered from vacuum exposure [19–21]. Vacuum-induced mutants showed a unique molecular signature of tandem-double base changes at restricted sites in the DNA [22]. This extremely dehydrating effect of space vacuum has been considered to be one of the factors that may prevent interplanetary transfer of life [23]. However, space experiments have shown that up to 70% of bacterial and fungal spores survived short-term, e.g.: 10 days, exposure to space vacuum, even without any protection [24]. The chances of survival

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Table 2. Survival rate of spores of B. subtilis after exposure to space vacuum (10–6–10–4 Pa) on board of SL 1, EURECA, and LDEF [24–26].

in space were increased if the spores were embedded in chemical protectants, such as sugars or salt crystals, or if they were exposed in thick layers. For example, 30% of B. subtilis spores survived a nearly 6-yr exposure to space vacuum if embedded in salt crystals, whereas nearly 70% survived in the presence of glucose (Table 2) [25]. It has been suggested that sugar or polyalcohol stabilizes the structure of the cellular macromolecules, especially during vacuum-induced dehydration, leading to increased rates of survival. In all experiments, ground controls were simultaneously subjected to vacuum at the space simulation facilities of the DLR. Survival rates of the ground controls were in most cases slightly higher than those of the space samples; however, this difference was not significant. Nevertheless, the damage to the DNA, observed in B. subtilis spores after exposure to space vacuum—as well as to vacuum in the laboratory—would accumulate during long-term interplanetary transfer, because DNA repair is not active in the dormant spore state. Survival would ultimately depend on the efficiency of the repair systems after rehydration and subsequent germination and growth. 3.3. Effects of Solar UV Radiation UV radiation is very potent in starting up various kinds of photochemical reactions in cellular systems, such as alteration/damage of proteins and DNA, which will interfere with proper cell function. The biological effectiveness of the different wavelengths of the solar spectrum is described by the action spectrum [27]. Particularly, UV–C (190–280 nm) and the short-waveband edge of UV–B (280–315 nm) radiation that do not reach the surface of Earth due to effective shielding by the stratospheric ozone layer are of high biological effectiveness (Fig. 3). Compared to the terrestrial UV radiation climate, the extraterrestrial UV spectrum was about 1,000 fold more effective in killing spores of B. subtilis [28,29]. This high biological effectiveness of extraterrestrial UV radiation is mainly caused by damage to the spore DNA induced by the UV–C part of the spectrum (Fig. 3). If the spores were simultaneously exposed to solar UV-radiation and space vacuum, they responded with an increased UV sensitivity (Fig. 3) [19,24]. This increased efficiency is caused by altered photoproducts generated within the desiccated DNA of B. subtilis spores when exposed to UV radiation in space vacuum [19,30]. It was concluded that these vacuum-specific photoproducts, which are less amenable to the DNA-repair processes, were responsible for the UV super-sensitivity of spores if irradiated under vacuum conditions [24]. However, it has recently been shown that spores within an artificial meteorite of about 1 cm in diameter were effectively shielded against the harmful impact of extraterrestrial solar UV radiation [31].

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Figure 3. Action spectrum of inactivation of spores B. subtilis by extraterrestrial solar UV radiation; results from space missions SL 1 and D2 and EURECA [26].

Figure 4. Biostack concept [35] to determine the biological effects of single HZE particles of galactic cosmic radiation.

3.4. Effects Galactic Cosmic Radiation The so-called HZE particles are the most biologically effective species of galactic cosmic radiation because of their extremely dense pattern of energy deposition [32,33]. Lesions in the biologically sensitive structures are produced with higher efficiency and prove less amenable to repair than those generated by sparsely ionizing types of radiation, such as x rays. Since the HZE particles in interplanetary space are present at very low abundance, e.g.: about 1/cm–2 day–1 at a LET>225 keV/μm [34], special methods must be developed for tracing their path within the biological system. The Biostack concept [35] consists of a sandwich-like structure where layers of biological objects, e.g.: bacterial spores, plant seeds, and insect eggs, are placed between nuclear track detectors (Fig. 4). This device al-

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lows the determination of the relative position of the HZE particle trajectory within the biological layer after processing (etching) the track detectors. The micron-sized spores of B. subtilis were the smallest biological specimens studied. It was found that the spores were inactivated well beyond a distance of 1 μm from the HZE particle track; however, even those centrally hit by an HZE particle had a 30% chance of survival [36]. Considering the low flux of HZE particles and the small size of bacterial spores, it may take up to 1 Ma before a spore is hit and damaged by an HZE particle when travelling through interplanetary space. 3.5. Assessment of Long-Term Survival in Outer Space Maximum exposure times in space, reached so far experimentally, were provided by the nearly 6-yr LDEF mission [25]. If arranged in thick layers, in the presence of sugars as chemical protectors, and shielded against solar UV radiation by 2 mm of aluminum, up to 70% of bacterial spores survived the 6-yr space journey (Table 2). However, the vast majority of rocks would need more than 10,000 yr, or even millions of years, to travel, for example, from Mars to Earth [37]. To assess the chances of microbial survival in outer space for such long lasting trips, two separate theoretical studies were recently performed [9,38]. Based on experimental data from laboratory experiments on radiation effects and DNA stability, they concurringly concluded that for such long travel times, boulder sized rocks ≥1 m in diameter are required to effectively shield resistant microorganisms, such as bacterial spores, against the impact of galactic cosmic radiation. However, one has to bear in mind that a very low fraction of Mars ejecta, in the order of 10–7, may reach Earth much faster, e.g.: in ≤1 yr after ejection [37]. For these fast transfers, the LDEF data are representative.

4. Landing on a Planet When captured by a planet with an atmosphere, most meteorites are subjected to very high temperatures during landing. However, because the fall through the atmosphere only takes a few seconds, the outermost layers form a kind of heat shield and the heat does not reach the inner parts of the meteorite. During entry, the fate of the meteorite strongly depends on its size. Large meteorites may brake into pieces, but the pieces may still be large enough to remain cool inside until hitting the surface of the planet. Medium sized meteorites may obtain a melted crust, but the inner part remains cool. Micrometeorites of a few microns in size may tumble through the atmosphere without being heated above 100 ˚C. Therefore, it is quite possible that a substantial number of microbes can survive the landing process on a planet. However, no experiments have been done so far to investigate the biological effects of the landing process. Recently, the European Space Agency has developed a facility, called STONE, which is attached to the heat shield of a FOTON satellite to test mineral degradations during landing. This facility might be an ideal tool to study the effects of landing of bacterial spores embedded in an artificial meteorite.

References [1] Arrhenius S. Die Verbreitung des Lebens im Weltenraum. Die Umschau 1903; 7: 481–5. [2] Horneck G. Could life travel across interplanetary space? Panspermia revisited. In: Rothschild LJ, Lister A, editors. Evolution on planet Earth: the impact of the physical environment. San Diego: Academic Press; 2003. in press.

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[3] Horneck G, Mileikowsky C, Melosh JH, Wilson JW, Cucinotta F, Gladman B. Viable transfer of microorganisms in the solar system and beyond. In: Horneck G, Baumstark-Khan , editors. Astrobiology, the quest for the conditions of life. Berlin-Heidelberg-New York: Springer-Verlag; 2002. p. 57–74. [4] Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microb. Mol. Biol. Rev. 2000; 64: 548–72. [5] Setlow P. Mechanisms for the prevention of damage to DNA in spores of Bacillus species. Ann. Rev. Microbiol. 1995; 49: 29–54. [6] Cano RJ, Borucki MK. Revival and identification of bacterial spores in 25 to 40 million-year-old Dominican amber. Science 1995; 268: 1060–4. [7] Vreeland RH, Rosenzweig WD, Powers DW. Isolation of a 250 million-year-old halotoleratn bactereium from a primary salt crystal. Nature 2000; 407: 897–900. [8] Horneck G, Stöffler D, Eschweiler U, Hornemann U. Bacterial spores survive simulated meteorite impact. Icarus 2001; 149: 285–90. [9] Mileikowsky C, Cucinotta F, Wilson JW, Gladman B, Horneck G, Lindegren L, Melosh J, Rickman H, Valtonen M, Zheng JQ. Natural transfer of viable microbes in space, part 1: from Mars to Earth and Earth to Mars. Icarus 2000; 145: 391–427. [10] Melosh HJ. Impact ejection, spallation and the origin of meteorites. Icarus 1984; 59: 234–60. [11] Melosh HJ. Ejection of rock fragments from planetary bodies. Geology 1985; 13: 144–8. [12] Mastrapa RMF, Glanzberg H, Head JN, Melosh HJ, Nicholson WL. Survival of Bacillus subtilis spores and Deinococcus radiodurans cells exposed to the extreme acceleration and shock predicted during planetary ejection. [abstract]. In: Proceedings of the 31st Lunar and Planetary Science Meeting; 2000; Houston. [13] Horneck G. Astrobiology studies of microbes in simulated interplanetary space. In: Ehrenfreund P, Krafft C, Kochan H, Pirronello V, editors. Laboratory astrophysics and space research. Dordrecht: Kluwer; 1999. p. 667–85. [14] Reitz G, Beaujean R, Heilmann C, Kopp J, Leicher M, Strauch K. Results of dosimetric measurements in space missions. Adv. Space Res. 1998; 22 (4): 495–500. [15] Labs D, Neckel H, Simon PC, Thuillier G. Ultraviolet solar irradiance measurement from 200 to 358 nm during Spacelab 1 mission. Solar Physics 1987; 107: 203. [16] Horneck G. Exobiological experiments in Earth orbit. Adv. Space Res. 1998; 22: (3)317–26. [17] Melosh HJ. The rocky road to Panspermia. Nature 1988; 332: 687–8. [18] Cox CS. Roles of water molecules in bacteria and viruses. Origins Life Evol. Biosphere 1993; 23: 29–36. [19] Horneck G, Bücker H, Reitz G, Requardt H, Dose K, Martens KD, Mennigmann HD, Weber P. Microorganisms in the space environment. Science 1984; 225: 226–8. [20] Dose K, Bieger-Dose A, Labusch M, Gill M. Survival in extreme dryness and DNA-single-strand breaks. Adv. Space Res. 1992; 12: (4)221–9. [21] Dose K, Bieger-Dose A, Dillmann R, Gill M, Kerz O, Klein A, Meinert H, Nawroth , Risi S, Stridde C. ERA-Experiment “Space Biochemistry”. Adv. Space Res. 1995; 16: (8)119–29. [22] Munakata N, Saito M, Takahashi N, Hieda K, Morihoshi F. Induction of unique tandem-base change mutations in bacterial spores exposed to extreme dryness. Mutat. Res. 1997; 390: 189–95. [23] Nussinov MD, Lysenko SV. Cosmic vacuum prevents Radiopanspermia. Origins Life Evol. Biosphere 1983; 13: 153–64. [24] Horneck G. Responses of Bacillus subtilis spores to space environment: results from experiments in space. Origins Life Evol. Biosphere 1993; 23: 37–52. [25] Horneck G, Bücker H, Reitz G. Long-term survival of bacterial spores in space. Adv. Space Res. 1994; 14: (10)41–5. [26] Horneck G, Eschweiler U, Reitz G, Wehner J, Willimek R, Strauch K. Biological responses to space: results of the experiment “Exobiological Unit” of ERA on EURECA I. Adv. Space Res. 1995; 16: (8) 105–11. [27] Jagger J. Introduction to Research in Ultraviolet Photobiology. Englewood Cliffs: Prentice Hall; 1967. p. 53. [28] Horneck G, Rettberg P, Rabbow E, Strauch W, Seckmeyer G, Facius R, Reitz G, Strauch K Schott JU. Biological dosimetry of solar radiation for different simulated ozone column thickness. J. Photochem. Photobiol. B: Biol. 1996; 32: 189–96. [29] Cockell CS , Horneck, G. The history of the UV radiation climate of the Earth—theoretical and spacebased observations. Photochem. Photobiol. 2001; 73: 447–51. [30] Lindberg C, Horneck G. Action spectra for survival and spore photoproduct formation of Bacillus subtilis irradiated with short wavelength (200 - 300 nm) UV at atmospheric pressure and in vacuo. J. Photochem. Photobiol. B: Biol. 1991; 11: 69–80.

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[31] Horneck G, Rettberg P, Reitz G, Wehner J, Eschweiler U, Strauch K, Panitz C, Starke V, BaumstarkKhan C. Protection of bacterial spores in space, a contribution to the discussion on Panspermia. Origins Life Evol. Biosphere 2001; 31: 527–547. [32] Horneck, G. Radiobiological experiments in space: a review. Nucl. Tracks Radiat. Meas. 1992; 20: 185– 205. [33] Kiefer J, Kost M, Schenk-Meuser K. Radiation biology. In: Moore D, Bie P, Oser H, editors. Biological and medical research in space. Berlin: Springer; 1996. p. 300–67. [34] Benton EV, Parnell TA. Space radiation dosimetry on U.S. and Soviet manned missions. In: McCormack PD, Swenberg CE, Bücker H, editors. Terrestrial space radiation and its biological effects. New York and London: Plenum Press; 1988. p. 729–94. [35] Bücker H, Horneck G. Studies on the effects of cosmic HZE-particles in different biological systems in the Biostack experiments I and II, flown on board of Apollo 16 and 17. In: Nygaard OF, Adler HI, Sinclair WK, editors. Radiation research. New York: Academic Press; 1975. p. 1138–51. [36] Horneck G. 1993. The Biostack concept and its application in space and at accelerators: studies on Bacillus subtilis spores. In: CE Swenberg, G Horneck, EG Stassinopoulos, editors. Biological effects and physics of solar and galactic cosmic radiation, Part A. New York: Plenum Press; 1993. p. 99–115. [37] Gladman BJ, Burns JA, Duncan M, Lee P, Levison HF. The exchange of impact ejecta between terrestrial planets. Science 1996; 271: 1287–392. [38] Clark BC. Planetary interchange of bioactive material: probability factors and implications. Origins Life Evol. Biosphere 2001; 31: 185–97.

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Reactions of Urazole and its Analogs with Sugars and Metals under Prebiotic Conditions Vera M. KOLB, Patricia A. COLLOTON and Kevin J. RAPP Department of Chemistry, University of Wisconsin-Parkside Kenosha, Wisconsin 53141-2000, USA Abstract. This work reports the selectivity of urazole, a prebiotic mimic of uracil, in its reactions with sugars. This selectivity is important in prebiotic synthesis of nucleosides. Urazole makes metal complexes. Thus, it may exist on meteorites as such. Some physical properties of urazole-metal complexes that are relevant for their recovery from the meteorites have been investigated.

Early and more recent [1–7] work has shown that urazole, a prebiotic analog of uracil with a comparable hydrogen- (H-) bonding ability to adenine (Fig. 1), readily makes nucleosides with ribose and deoxyribose under prebiotic conditions, in the aqueous medium. Urazole reacts with ribose and deoxyribose in a regioselective manner. A single substitution on a hydrazidic nitrogen (N) occurs and reaction on the imide nitrogen is observed. A mixture of four nucleosides, α and β pyranosides (p), and α and β furanosides (f) is obtained. This reactivity pattern of urazole leaves its imide group, C=O-NH-C=O, free and available for H-bonding with adenine. Urazole distinguishes between ribose and deoxyribose in a significant way: with ribose it gives predominantly the β-p nucleoside, while with deoxyribose it provides the α-p nucleoside. In the reaction of 2-deoxyribose with urazole or its cyclic analogs, such as 4methylurazole and 4,4-dimethylpyrazolidine-3,5-dione, a crystalline precipitate, which is an exclusive enantiospecific product, 1R, 2R α-p, as determined by x-ray studies [2,3,5] (Fig. 2) is formed. Urazole with 2-deoxy-L-ribose gives a precipitate with the exclusive 1S,

Figure 1. (a) Urazole and (b) uracil.

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Figure 2. Summary of work on the reactions of urazoles with sugars.

2 S α-p stereochemistry [6]. Therefore, the stereochemistry of deoxyribose influences that of the urazole's hydrazidic nitrogens in the nucleoside that is formed. With 2-deoxy-Dglucose the reaction with urazole is stereospecific, since only one isomer, β-p, forms in solution [7]. The summary of these reactions is given in Fig. 2. The α-effect in the reaction of urazole with sugars was also studied. This effect predicts an enhancement in the nucleophilic reactivity of the -NH-NH- unit in urazole due to the interaction of lone-electron pairs on the neighboring nitrogens. It was found that the cyclic analogs of urazole, such as 4-methylurazole and 4,4-dimethyl- pyrazolidine-3,5-dione, are reactive, but the open-chain analogs, such as 1,2-diacetylhydrazine and 1,2-dicarbethoxyhydrazine, are not. Therefore, these open-chain analogs will not compete with urazole for sugars in the prebiotic medium [4,7]. A representative experimental procedure for the synthesis and isolation of the urazole nucleosides can be found in the work by Robinson et al. [2]. The selectivity of the reactions of urazole with sugars is of great prebiotic importance. Instead of a combinatorial mixture of the nucleosides, specific nucleosides are preferred in the reaction mixtures, and only one may crystallize out. This is an unanticipated, but welcome result of the chemical evolution. Whether or not urazole nucleosides make complexes with metal salts at the natural pH at which they are formed, which is acidic (under the basic conditions sugars decompose) is of great intrest. Such complexation could stabilize the nucleosides or impart to them some catalytic properties. The first step was to study the complexation of urazole. Urazole, indeed, forms complexes with metals under the acidic conditions, including cobalt (Co), nickel (Ni), silver (Ag), and zinc (Zn) [8,9]. Others have shown analogous complexation of guanazole [10,11], and doubly deprotonated urazole under the basic conditions [12]. Since urazole and guanazole are important prebiotic molecules, whose prebiotic syntheses have been demonstrated [1], it is suspected that they may be present on meteorites. However, a question arises: Can these molecules be easily detected if they make complexes with various metals that may be present on meteorites? Such complexes need to be broken up during the extractions of organics from the meteorites in a manner that does not chemi-

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cally change the parent ligands, urazole and guanazole. Otherwise, one would miss a possible presence of these compounds on meteorites. Reported here are the preparation, some physical properties, and solubility of these metal complexes, which are believed to be relevant for the problem of their recovery from meteorites. All starting compounds were from commercial sources (Sigma Aldrich and Fisher): Guanazole (3,5- diamino-1,2,4-triazole), urazole (1,2,4-triazolidine-3,5-dione), cobalt (II) nitrate (Co (NO3)2 • 6H2O), nickel (II) nitrate (Ni (NO3)2 • 6H2O), silver (I) nitrate (Ag NO3), and zinc (II) nitrate (Zn (NO3)2 • 6H2O). The complexes of guanazole were prepared by the published method [10,11]. The same method was adapted for the synthesis of urazole complexes, as shown below. The previously published procedure was not followed for the reactions of the doubly deprotonated urazole with the metal salts in which buffers were used to bring the pH up to ~8 [12]. In contrast, for this effort, the reaction was performed under natural pH, which is acidic, for both urazole and the metal salts that were used (pH was ~4). Urazole (0.354 g, 3.5 mmol) was dissolved in warm water (1.5 ml) and acetone (8.0 ml). The Co, Ni, or Zn nitrates (0.5 mmol) were each separately dissolved in acetone (2.0 ml) (for Ag nitrate a small volume of water was also added). The metal nitrate solution was added to the urazole solution and refluxed for 30 min. During this time, a precipitate formed, which was suction filtered, washed with acetone, and dried. (In the case of Ag nitrate, an immediate precipitate formed.) The IR spectra of the complexes were taken in the Nujol mull and also as KBr powder (reflectance method). What follows is a summary of our results for KBr powder. The IR spectra of the urazole complexes indicate that urazole interacts with metals via its carbonyls. Urazole’s carbonyl shows a strong band at 1,692 cm–1. In some complexes, this band shifts towards lower frequencies, e.g.: in Zn, 1,686 cm–1, strong; Co 1,681 cm–1, strong). In some other complexes, the band moves towards higher frequencies but is accompanied by a strong band at a lower frequency, perhaps indicating some type of vibrational coupling (Ag, 1,710 cm–1, strong, 1,634 cm–1, strong; Ni 1,714 cm–1 strong, 1,605 cm–1, strong). These IR frequencies are different than those reported for the complexes of doubly deprotonated urazole [12], as expected. The melting points of all the urazole complexes are quite high. Most of them did not reach the point of melting or decomposition at 300 ˚C, except for the silver complex that decomposed at 236–240 ˚C. The solubility’s of urazole complexes were measured qualitatively, by solubility criteria of a couple of milligrams of a complex in 2 mL of water, 5% HCl, or 5% NaOH. All complexes were insoluble in water, and they were only slightly soluble or insoluble in 5% HCl or 5% NaOH. In the latter, the Ag complex reacted to give a silver mirror. Guanazole is known to exist as a mixture of several tautomers (Fig. 3). The IR spectra of the guanazole metal complexes are substantially different from the spectra of guanazole but do not unambiguously point to the tautomer(s) that reacts. These spectra are in a general agreement with previously published spectra [10]. Solubility of guanazole complexes is similar to that of the urazole complexes. Other authors [10] have proposed that in the complexation of guanazole with metals the ring nitrogens act as donor atoms due to a charge distribution. To confirm this, higher level calculations have been performed (ab initio) on the various tautomers of guanazole (Fig. 3). The electrostatic potential surfaces and HOMO and LUMO pictures indicate that the sp2 hybridized ring nitrogens indeed have favorable electron-density distribution for complexation. In conclusion, these results indicate that urazole has a good ability to complex with various metals. It does so via its carbonyl form. Guanazole, which also forms complexes, reacts in one or several of its tautomeric forms. Guanazole probably reacts via its ring sp2

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Figure 3. Guanazole tautomers.

nitrogens. Due to the complexing ability of these two molecules with metals, they may exist on meteorites as metal complexes, and special procedures may be needed to isolate these compounds from meteorites.

Acknowledgments The Wisconsin Space Grant Consortium/NASA, to whom gratitude is expressed, has sponsored this work. Thanks are expressed to Cal Y. Meyers and Paul D. Robinson for the x-ray studies and a continual interest in this work. Special thanks are due to Randall Stewart Perry for discussions of the astrobiological potential of our work with metal complexes.

References [1] Kolb VM, Dworkin JP, Miller SL. Alternative bases in the RNA world: the prebiotic synthesis of urazole and its ribosides. J. Mol. Evol. 1994; 38: 549–57. [2] Robinson PD, Meyers CY, Kolb VM, Colloton PA. First example of a crystalline urazole nucleoside. (1R, 2R)-Urazole-αα-D-pyranosyl-2-deoxyriboside. Acta Cryst. 1996; C52: 1215–8. [3] Kolb VM, Colloton PA, Robinson PD, Lutfi HG, Meyers CY. (1R, 2R)-4,4-Dimethylpyrazolidine-3,5dione-α-D-pyranosyl-2-deoxyriboside. Acta Cryst. 1996; C52: 1781–4. [4] Kolb VM, Colloton PA. On the mechanism of formation of urazole nucleosides: reaction of open-chain and cyclic analogs of urazole with D-Ribose and 2-Deoxy-D-ribose. In: Moore GT, Brandt SD, editors. Mission to planet Earth. Milwaukee: Wisconsin Space Grant Consortium;1997. Part II. [5] Meyers CY, Hou Y-Q, Kolb VM, Robinson PD. (1R,2R)-4-Methyl-α-D-pyranosyl-2-deoxyriboside from reaction of 4-Methylurazole with 2-Deoxy-D-ribose. Acta Cryst. 1997; C53: 1502–5. [6] Robinson PD, Kolb VM, Colloton PA, Meyers CY. First Example of a Crystalline Urazole Nucleoside with an L-Configured Sugar. (1S,2S)-Urazole-α-L-Pyranosyl-2-deoxyriboside. Acta Cryst. 1997; C53: CIF, QP00003, IUC9700004. [7] Kolb VM, Colloton PA. manuscript in preparation. [8] Kolb VM, Colloton PA, Rapp KJ. Abstract 5–5. Second Florida Heterocyclic Conference. Gainsville, Florida; 2001.

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[9] Kolb VM, Colloton PA, Rapp KJ. Abstract 36. RNA Based Life Conference. Bloomington, Indiana; 2001. [10] Gabryszewski M, Wieczorek B. Syntheses and properties of the Co(II), Ni(II), Zn(II) and Cd(II) complexes with 3-amino-1,2,4-triazole, 4-amino-1,2,4-triazole, 3,5-diamino-1,2,4-triazole and 3-amino-5methylthio-1,2,4-triazole. Polish J. Chem. 1999; 73: 2061–6. [11] Gabryszewski, M., and Wieczorek, B., (1998), “Silver (I) complexes with 1,2,4-triazole, 1-ethyl-1,2,4triazole, 3-amino-1,2,4-triazole, 4-amino-1,2,4-triazole and 3,5-diamino-1,2,4-triazole”, Polish J. Chem., 72, 2352–3. [12] Batyr DG, Baloyan BM, Popa EV, Kharitonov YuYa. Coordination compounds of manganese (II), iron (II), cobalt (II), nickel (II), copper (II), and zinc (II) with hydrazodicarbonimide (urazole). Koord. Khim. 1981; 7: 598–604.

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Apatite as Biosignature Jüri NEMLIHER Institute of Geology, Tallinn Technical University, Estonia Estonia pst 7, 10143 Tallinn, Estonia [email protected] Abstract. An overview of biomineralization processes is given with special respect to phosphatic minerals formation. The properties of Phanerozoic apatite biominerals are described as being a biosignature of high rank.

Introduction According to definition, biomineralization is a process during which a mineral phase generation takes place due to biological activity of organisms [1]. The referenced work reports a total of 31 biogenic minerals, while to date the number of known mineral modifications, which can be attributed to biomineralization, has increased to more than 200 (from lectures on the Astrobiology Conference, Chania 2002). Most belong to minerals formed due to microbial activity. Considering the rank of biological control over mineral phase formation, a sort of gradation might be constructed [1], from induced to matrix mineralization (Fig. 1). On Earth, the first known matrix mineralization occurrence is Cloudina from the Upper Proterozoic of Namibia [2]. Starting from Early Cambrian, the skeletal biomineralization has become abundant and characteristic of many taxonomic groups, extinct and living. The

Figure 1. Schematic drawing, illustrating relationships between biological control and mineral homogeneity and bodies, formed during this process.

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most common biominerals are silica (opal), calcite, aragonite, and apatite. Considering the rank of variability of those mineral modifications, the most stable form is silica, where substitutions are absent; calcium-carbonates of biological origin might be estimated to tolerate 0.1% of lattice parameters variations due to substitution of Sr and Magnesium into mineral. The most flexible mineral is apatite, where the range of lattice parameter variations is as high as 6%. The large range of lattice parameter variability is by reason of very large chemical substitutions into the mineral lattice as well as into different positions [3,4]. Among the most important substitutions, OH, chlorine, and CO3, should be noted, because the amount and position in the apatite lattice generally cause the observable crystallochemical properties [5]. Alongside the crystal lattice reticularis, the other characteristic features of bioapatite properties on the sub-atomic level are strains, content, and crystallite dimensions. Those characteristics fall into range, they are best observed using the x-ray wavelength. In this paper, an overview of bioapatite is given, ascribing those features that might be treated as biosignatures.

1. Apatite Biomineralization Apatite is considered to be one of the oldest biominerals. According to stable isotope studies, possible biogenic origin has been attributed to 3.85–3.80 Ga old apatite from the Akilia and Isua formations in Greenland [6]. This evidence has been regarded as a possible trace of the earliest life on Earth [7]. From the point of view of origin, the majority of the phosphate deposits on our planet are related to products of induced mineralization mechanisms. During geological history, the biogeochemical pathways of this sort of mineralization have been completely changed. In spite of that, completely different trophic pathways of microbiota involved into formation of e.g. Khubsugul cyanobacterial phosphorates versus Holocene upwelling phosphorites (Zavarzin, pc), resulted as the same mineral modification [8]. Since the Cambrian, the matrix-mineralized phosphate became common. The bestknown mass-accumulation of skeletal, primarily phosphatic, remains are related to the Upper Cambrian in Northwest part of the East European Platform (Obolos-Phosphorites), forming phosphorite deposits of commercial interest [9]. These data are based on the whole-pattern fitting of x-ray detection (XRD) patterns, as described in Nemliher and Kallaste [10]. Some XRD patterns of apatite modifications formed by different participation of biological mechanisms are shown on Fig. 2. Basically, observable XRD patterns contain information on lattice parameters and crystallinity, which can be divided into strain component and component, caused by tiny dimensions of crystals of individual samples.

2. Lattice Parameters Lattice parameters represent a reticularis of atoms in a particular lattice direction and can be regarded as a co-function of chemical composition. Considering the published data on different apatite modifications [4], most lattice parameter variations can be attributed to amounts of and relationships between these particular ions, i.e.: as fluorine (F), OH and CO3. A scatter plot of lattice parameters of apatite modifications and differing origin is shown in Fig. 3, showing a certain taxa-specificity of mineral modification. Also, taxaspecific composition of bioapatite can be correlated with the phylogenetic age of the same

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Figure 2. Untreated XRD patterns (Co-radiation, λ=1.788965 Å) of some apatite modifications, ordered by the degree of biological control: (a) Hydrothermal carbonate-F-apatite from Staffel, Germany; (b) sedimentary apatite of Middle Ordovician, Estonia; (c) apatite of shell of Recent Discinisca striata, Lüderitz, Namibia; (d) apatite of bones of recent squirrel (Sciurus vulgaris), Estonia; (e) apatite of archaeological human enamel, St. Barbara Cemetery, 14th century, Estonia; (f) apatite of conodonts, Lower Ordovician, Estonia.

group; the most recent groups of skeletons built up of apatite with the highest OH content. On the other hand, apatites of endogenic as well as metamorphic origin have lattice parameters that resemble F-apatite [4], thus the area of biogenic apatites is a somewhat connected to biota.

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Figure 3. Scatter plot of lattice parameter values of different recent skeletal apatites and Holocene upwelling phosphorites [11,12].

Figure 4. Calculated average crystallite dimensions of some bioapatites: (a) Shell, mineral, and dentine; (b) enamel (enameloid) tissues.

3. Crystallinity The crystallinity of studied samples shows significant differences between bioapatites and those formed during endogenic processes. The last are built up of crystallites, whose dimensions in both lattice directions always exceed thousands of angstroms while skeleton parts consists of particles, whose dimensions are tens or hundreds of angstroms. Sedimentary apatite varieties are somewhat intermediate, however, tending to be closer to bioapatites. In spite of the visual similarity of XRD patterns of, for example, a conodont apatite (Fig. 2(f)) and a hydrothermal one (Fig. 2(a)), the profile shape function, which satisfactorily matches the conodont XRD reflections, is much more complicated and consists of two

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bell-shaped functions, which are represented by modified Lorentzians. The most complicated hard tissues, such as enamel and different enameloids, are built up of two crystallites series, one of which is similar to a dental type while the other is around 10 times larger (Fig. 4). Both crystallites are represented by discrete series.

4. Bioapatite Properties as Biosignature Considering the astrobiological definition of biosignature as being “any measurable property of a planetary object, its atmosphere, oceans, geologic formations, or sample that suggests that life is or was present” (McKay, from lecture on the Astrobiology Conference, Chania 2002), the complex mineral properties are well suitable as being detected as a biosignature. The properties of ferric minerals have been considered as biosignatures of life activity of magnetotactic bacteria [13,14]. In this light, the properties of apatite mineral deserve serious attention as a biosignature. Moreover, combination of lattice parameters values with crystallinity, described above, should be treated as a biosignature of high rank.

Acknowledgements This work is supported by ESF (Grant No. 5275).

References [1] Lowenstam HA. Minerals formed by organisms. Science 1981; 211: 1126–1131. [2] Grant SWF. Shell structure and distribution of Cloudina, a potentional index fossil for the terminal Proterozoic. Am. J. Sci. 1990; 290 A: 261–294. [3] Elliott JC. Structure and chemistry of the apatites and other calcium orthophosphates. AmsterdamLondon-NY-Tokyo: Elsevier; 1994. [4] McConnell D. Apatite—its crystal chemistry, mineralogy, utilization and geologic and biologic occurrences. Vienna-Heidelberg-New York: Springer; 1973. [5] Puura I, Nemliher J. Apatite varieties in recent and fossil linguloid brachiopod shells. In: Brunton CHC, Cocks LRM, Long SL, editors. Brachiopods past and present. The Systematics Association Special Volume Series 2001; 63: 7–16. [6] Moijzis SJ, Arrhenius G, McCeegan KD, Harrisson TM, Nutman TM, and Friend CRL. Evidence for life on Earth before 3,800 million years ago. Nature 1996; 384; 55–59. [7] Gedulin B, Arrhenius G. Sources and geochemical evolution of RNA precursor molecules: the role of phosphate. In: Bengston S, editor. Early life on Earth. Nobel Symp. 84. New York: Columbia Univ. Press; 1994. p. 91–106. [8] Nemliher J. Mineralogy of Phanerozoic skeletal and sedimentary apatites: an XRD study. Dissertationes Geologicae Universitas Tartuensis 1999; 8: 1–47. [9] Trappe J. Phanerozoic Phosphorite depositional systems. A dynamic model for a sedimentary system. Springer 1998: Lecture Notes in Earth Sciences; 76. [10] Nemliher J and Kallaste T. Post mortem alteration of shell apatite of Discinisca tenuis from Lüderitz, Namibia. Lithol. & Min. Res. 2002; 37: 18–24. [11] Nemliher J, Kallaste T, Puura I. Hydroxyapatite varieties in recent fish scales. Proc. Acad. Sci. Estonia. Geology 1997; 46: 187–96. [12] Nemliher J, Baturin GN, Kallaste T, Murdmaa IK. Alteration of OH-apatite from seafloor during fossilization. Lithol. & Min. Res., 2003; 38: in press. [13] Thomas-Keprta KL, Clemett SJ. Truncated hexa-octahedral magnetite crystals in ALH84001: presumptive biosignatures. Proc. Nat. Acad. Sci. USA, 2001; 98: 2164–70. [14] Thomas-Keprta KL, Clemett SJ, Bazylinski DA, Kirschvink JL, McKay DS, Wentworth SJ, Vali H, Gibson EK, Romanek CS. Magnetofossils from ancient Mars: a robust biosignature in the Martian meteorite ALH84001. Appl. Environ. Microbiol. 2002; 68: 3663–72.

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Tikhov’s Astrobotany as a Prelude to Modern Astrobiology Tuken B. OMAROV and Bulat T. TASHENOV Astrophysical Institute, Almaty, 480020 Kazakhstan Abstract. Development of astrobotanical research by G.A. Tikhov in the Kazakh Academy of Sciences is considered seminal to today’s astrobiology.

In 1949, in Kazakhstan, Gavriil A. Tikhov published a book entitled “Astrobotany” [1]. Later in 1953, the author published a paper, “The Possibility of Life in the Other Worlds” [2] and a book “Astrobiology” [3]. These works of Tikhov were the results of research activity by the Section of Astrobotany, founded in 1947 at the Academy of Sciences of Kazakhstan. Tikhov was an eminent astrophysicist. As early as 1906, he began his astrophysical researches at the Pulkov Observatory, which is located in suburb of St. Petersburg. In particular, his suggestion to employ coloured filters for planet observation had an important role in the development of planetary science as a whole. By 1909 he obtained the first images of Mars in different light spectrums. This allowed him to find a difference in the size and brightness of visible objects on Mars in different spectrum segments. As an astronomer, who, from his early years, believed in the existence of life on Mars, he tried unsuccessfully to detect, on the spectrograms, a major absorbency spectrum of chlorophyll that is very characteristic for Earth’s plant surface. Tikhov was convinced that life is an extremely persistent and stubborn matter, and therefore, he wondered whether the absence of the absorbency spectrum of chlorophyll in Mars’ spectrograms is due to extreme climatic conditions. At conditions of very low ambient temperature, the absorbency spectrum of chlorophyll can be very extended; it would not be possible to detect it using the reflected signal of plants that hypothetically could grow on Mars. This may be the result of decreased spectrum of chlorophyll absorbency and, simultaneously, increased levels of solar energy absorbency. In 1945, while working in Kazakhstan, Tikhov decided to investigate this question through a detailed study of the optical properties of plants growing in different climatic zones of Earth. During the same year, the first scientific expeditions the Section of Astrobotany were launched. This was possible due to the vigorous support of the president of the Kazakh Academy of Science at that time, K.I. Satpaev. Indeed, with time, such expeditions confirmed that in harsh climatic zones, the absorbency spectrum of chlorophyll becomes smeared and, sometimes, even disappears, as it was reported for Canadian fir. Therefore, in the early 1950s, Tikhov dismissed a main argument against the possibility of life on Mars; it was the beginning of the active introduction of astro-spectrophotometry methods to botany. In fact, the fluorescence in the infrared spectrum and other optical features of plant material were demonstrated for the first time during this period. Simultaneously, a sophisticated and unique spectrophotometer for field experiments was developed and constructed in

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the Section of Astrobotany. This allowed scientists to detect spectral features of plants in situ without traditional mechanical destruction of the given plant material. Tikhov was also planning to construct a special climate chamber for imitating climatic conditions on Mars. Interestingly, the question of the possible creation of an organization of a special Observatory of Planets at Section of Astrobotany was discussed during that period. In Almaty, Leningrad, and Moscow the research activity of Section of Astrobotany was widely argued and discussed. Interestingly, this polemic further strengthened Tikhov’s scientific ideas and beliefs. However, he died in 1960. And later, in 1964 when K.I. Satpaev passed away, the scientific activity of Section of Astrobotany was completely terminated. The first achievements in space research did not provide optimistic results regarding the possibility of life on the planets of the solar system. At that time, many scientists took a very negative approach towards Tikhov’s ideas. Remarkably, a scientific plan from the Section of Astrobotany contained a paragraph entitled “Programming of Living Conditions on the Planets.” Tikhov believed that the study of the possibility of life on Mars as a research subject of the Section of Astrobiology is a part of the fundamental problem of life expansion in the universe. In 1953, Tikhov considered the feasibility of the occurrence of living organisms on the planets of the solar system. According to his opinion, the question of the possibility of life existing on other planets should be considered on the basis of the following main points: • • •

Laws of life in the universe are generally ubiquitous but unique by their emergence. Adaptability of living organisms to different conditions is extremely high. Plants have an optical adaptability to different environmental conditions.

Tikhov determined that so-called biological geo-centrism was be a point of view that accepts the possibility of life exclusively on Earth. The ideas of Tikhov should be revisited based on continuing and developing studies of the solar system using modern space technologies paralleled with expanding interest in the question of the possibility of the existence of life on other planets. In particular, some astronomers and biologists are of the opinion that the current research efforts should be focused on the relatively small moons of Jupiter and Saturn. Nowadays, astrobiology is active again as the science of the forms and development of life in extreme conditions, distinctive for the Earth and other planets. During recent years, these studies have brought new arguments and an important conclusion that the area in which life exists on the Earth turns out to be much wider than it was earlier presumed to be. At NASA’s Ames Research Center, the Institute of Astrobiology has been opened, and very frequent scientific conferences are being organized worldwide by NASA, the European Space Agency, and others. Tikhov’s seminal work provides significant guidance to today’s astrobiologists, and his publication, “Astrobotany as a Prelude of Astrobiology” [4], is recommended to the participants to this ASI.

References [1] Tikhov GA. Astrobotany. Acadamy of Science, Kazakh: Alma-Ata; 1949. p. 23. [2] Tikhov GA. The possibility of life in the other worlds. In: Proceedings of the Astrobotany Section: AlmaAta; 1953:1. [3] Tikhov GA. Astrobiology. Moscow: Molodaya gvardia (Young Guard); 1953. [4] Tikhov GA. Astrobotany as a Prelude of Astrobiology.

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Computation of Sediment Cycles on Mars and Earth Elfi Van OVERLOOP and Roland PAEPE GEOBOUND INTERNATIONAL Research Center, Doornstraat, 27, B-9550 Herzele, & Free University of Brussels, Belgium Abstract. Many earlier attempts for computing periodicities in Mars sediment time series have proved to be quite successful with the Expert System for Spectral Analysis on continental deposits (ExSpect)—Matlab or Autoregressive (AR) Power Spectral Density (PSD) Cyclicity Calculation Method. The method was originally worked out for sediments interfering with datable key beds and fossil soil levels in recent (<2.4 Ma) deposits on Earth. Numerous time-bound (climatic) parameters could therefore be used on earth sediments. Since neither Mars sediment nor Mars sediment-boundary ages are known, recourse was taken to the relative sediment deposit genetic rate (RSDGR) as a standard parameter. For the purpose of the NATOASI course, different types of Mars images were selected, e.g.: images from sole ice layers of polar caps and images of sediment series performing permafrost features (cryoturbation levels, ice blocks, solifluction layers, etc.) indicating Earth-like climatic changes. The very latter can thus offer suggestions about the time-range that such climate changes may then represent. The results of cycle computation made on this basis were compared to those made for similar deposits on Earth. Since both were revealed to be highly comparable, the idea of cyclicities in resonance for both planets is hereby suggested and represented in tables at the end of this paper.

Introduction On Earth, the systematic search for climatological and astronomical periodicities is a longtime tradition. Solar radiation cycles became famous by the name of Milankovitch cycles [1] for the eccentricity (~100 Kyrs), obliquity (~41 Kyrs), and the precession (about 19 to 23 Kyrs). In geology, the same tradition has existed since the end of the 19th century for marine deposits. By the end of the 20th century, deep-sea marine sediments were moreover the subject of oxygen isotopic analysis of the parameters, which enabled Shackleton [2] to set up cyclicities, again revealing, quite surprisingly, the Milankovitch cycles. The same was found in the ice cores of Greenland and Antarctica. Thus, it became evident that climate-astronomical changes were reflected in geological deposits. Besides, deep-sea and ice cores offer records of the volume, intensity, and frequency of the growth of land ice. Other geological land deposits became the subject of cycle research, as well, especially in areas with thick, uninterrupted sequences of windborne sediments as on the loess plateau in China. Also, carrying out spectral analysis on the grainsize parameter, Liu [3] could prove that Milankovitch cycles control the loess sedimentation time series. Furthermore, based on the paleomagnetic evidence of reversals and events, Liu could show that a perfect correlation could be established between the deep-sea marine deposits and the continental loess deposits. Therefore, the global climatic-environmental character of Earth’s cycles was definitely proved.

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As explained elsewhere in this volume by Paepe and Van Overloop [4], it was found that fossil soils (geo-soils) occupy a soil stratigraphic stable position in land sediment series. However, unlike the case of loess deposits, geosoils seldom occur in sediment series suitable for spectral analysis. Actually, most of the soil series occur in coarse-grained to gravely heterogeneous deposits of the tropical and subtropical regions of the world, the latter covering vast areas of the world in comparison to the smaller, typical loess belts of China, Kazakhstan, Central and Western Europe, and the Midwest of the United States. If soil stratigraphic series could be made suitable for spectral analysis in all these regions, then climatic-astronomical cycles are likely to be computed for almost every spot of the entire world; thus, a better insight would be gained of the climate-environmental evolution of Earth. For this purpose, Van Overloop developed [5] ExSpect in the period from the late 1980s to the middle 1990’s [6–8] referring to numerous sites located all over the world. It was thanks to the UNESCO-International Postgraduate Training Program on Fundamental and Applied Quaternary Geology (IFAQ) that this multilateral project could be set up in China, Southeast Asia, Central Asia, the Middle East, the Mediterranean, and Central Africa in which more than 25 postgraduate geologists from different countries were participating. During this research project, the ExSpect method was applied to a threefold system of land sediment series. The latter was established by Paepe and Van Overloop [9] splitting up the time-span of the Pleistocene Ice Ages in: the Long-Term (Pleistocene) Series of 2.4 Ma, the Middle-Term (Last Interglacial-Last Glacial 127 Ka) Series and the Short-Term (Holocene 10 Ka) Series (Fig. 1). These three time sections of soil-sediment series correspond with specific cyclicities that deal with the combined effect of astronomical, solar, and planetary parameters. From these land geo-soil sequences a great number of cycles, besides the classical Milankovitch cycles, were computed, which, in order of importance, are 31, 62, 13, 11, 20, 51, 35, 55, 76, 89, and 127 Ka. The latter cycles may appear as half values of the current Milankovitch cycles or in combination with other astronomical and planetary cycles typical of the ShortTerm cycles. As it became clear that Earth’s cycles are controlled by solar and planetary parameters, two evident question were raised: (1) Are the same cycles found to control Mars and (2) were the same forcing agents acting? This is the purpose of this contribution to “Perspectives in Astrobiology”. For, if Earth’s environment is a direct consequence of climatically biased solar and planetary parameters, it can immediately be suggested that the same astronomical forcing had an impact on all other planets of our solar system and, specifically, Earth’s closest neighbor, Mars. This suggests another series of relevant questions, especially with regard to the simultaneous effect of a possible common impact of astronomical, solar, and planetary forcing on all planets of our solar system. Does this imply a kind of resonance in the planetary evolution of our solar system, a common start followed by different pathways of evolution for each of the planets concerned, or a specific common evolution of Earth and Mars? The answers could eventually explain the features of melting at the surface of Mars today, synchronous to the ones currently observed on Earth.

1. The ExSpect Methodology Developed on Sediment Series of the Earth 1.1. Concept of the ExSpect Methodology In order to bring about the ExSpect methodology, it was tested on various sediment series of Earth as mentioned in the introduction. Most important was the control of the ExSpect

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Figure 1. The threefold subdivision of fossil soil-sediment time series for the last 2.5 million yr.

methodology on Shackleton’s deep-sea records in which cycles had already been computed before by other computation methods especially developed for sediment series, which were

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believed to form a continuous depositional series and not be interrupted by standstills such as geo-soil horizons. Indeed, geosoils are standstills in the sedimentation process and may disturb the continuity in the depositional character of any sediment series. In the deep-sea sediments, the sedimentation process is, in fact, going on continuously without any major interruption. Paepe showed that geosoils in sediment series are definitely time-stable horizons in the sediment sequence [10]. This means that geo-soil levels occupy a definite time-stratigraphic position whatever its geographical location. This evidence resulted from the correlation of numerous Pleistocene geological sections recorded by IFAQ researchers in many regions of the tropical and subtropical world as well as from the more boreal locations studied in loess sections. Ultimately, Fig. 1 shows the summing up of this correlation, carried out for each the three series (long, middle, short) of time stable geo-soils: 67 (interglacial) geosoils for the Long-Term Pleistocene record of 2.4 Ma, 13 (interstadial) geosoils for the Middle-Term Last Interglacial-Glacial record of 127 Ka, and 20 modern geosoils for the Short-Term Holocene record of 10 Ka. These geosoils occupying time-stable stratigraphic positions in all three sediment sequences obey a stochastic process in (sediment) time series. Hence, they are reference or key beds, which can be used in spectral analysis for computing cycles, cyclicities, cycle boundaries, and even relative geological ages. Most astronomical and climatic modelers, being unaware of the stochastic nature of these geodynamic soil-sediment processes, hitherto failed to use them in classical modeling based on Milankovitch’s orbital changes of the Earth (eccentricity, obliquity, and precession). Instead, they solely were using preconceived idealized models based on a (restricted) number of parameters that were equally preconceived or presumed. In order to abandon the trial-and-error method in cycle computation, and in order to obtain real climatic cyclicities suitable for indication of the environmental evolution, an absolute computing program based on geological proxy-data was needed and established by the ExSpect methodology, designed in Matlab and based on stochastic series, such as the geosoils and related sedimentological data. In order to test the global climatic validity of the method, it was not only tested in various locations of different climatic regions but for different parameters as well: pollen, grain-size, oxygen isotopic compounds, carbonate content, etc. 1.2. Validity of the ExSpect Method as a Direct Computing Method Mathematically, the ExSpect method is also the result of testing a broad area of spectral algorithms and estimators. Keeping the stochastic behavior of geosoils (or any other sedimentary key-bed) in mind, the choice of the best adapted PSD algorithm was developed from all kinds of sediments used for detecting cyclicities hidden in the geological parameters on Earth. Indeed, for very short data records obtained from stochastic processes, classic spectrum estimators, such as those originating from the discrete fast Fourier transformation (FFT), yield very weak performances. The more powerful, modern spectrum estimators, which are available today, are based on a parametric modeling approach. The AR, movingaverage (MA), and the combined auto-regressive moving average (ARMA) models are enable the estimation the PSD of stochastic processes. Ultimately, the best fitting algorithm for geological processes appeared to be a discrete FFT interacting with an AR Burg algorithm for which a Levinson application on a Toeplitz matrix yielded the best results. In order to check the validity of the ExSpect method, the Earth’s orbital Milankovitch cycles as well as the Long-Term series of ODP 677 deep-sea cycles were recalculated and proved to filter out correctly. In younger deposits (<127 Ka), smaller cycles having an impact on Earth’s climate, i.e.: planetary periodicities and resonances, sunspot cycles and the Sun’s orbital cycles, could also be calculated and also proved to respond to Fairbridge’s planetary cycles [11]; thus, confirming the validity of the shorter cyclicities, as well.

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Figure 2. Example of frequency peaks as shown as a periodogram on-screen. There are five reliable peaks (the very first ones); the other peaks are clearly separated: they represent white noise.

1.3. Data Preparation and Implication Since the detection of cyclicities is a performed time signal or stochastic processing approach, the need for equidistance for the continental geological proxy data was another requirement to be fulfilled. In the stratigraphic column geologic layers and geosoils in particular, most often, do not show an equidistant display. Therefore another program in MatLab, called Interpolgeo was conceived for the very purpose of the interpolation of the proxy data. Thus, conditions for equidistance and requirements to apply the Shannon-Nyquist theorem (needed for both FFT and autoregressive algorithms) could be met. Since all sampling processes must obey to the latter theorem, it means that for geologic processes sampled at frequency f, the spectral information will only be available to a degree of f / 2. Interpolgeo is applied to the raw data in order to stretch the data set until the required number of proxy-data points and the required number of Shannon-Nyquist points are obtained. ExSpect is then progressing in following steps: 1. 2. 3. 4.

Data are first transformed to satisfy equidistance using Interpolgeo. The AR Burg Model is applied after the FFT as a robust spectrum estimator. For the estimator, a model order is selected in order to obtain the best results. Frequencies of peaks in the PSD are estimated and plotted; the noise is clearly separated from the reliable peaks. 5. Frequency peaks are detected, and their value is measured on-screen on the periodogram (Fig. 2). The next step is estimator and the frequency peak interpretation. Initial visual inspection of the periodogram leads to the indication of a periodic behavior. From this plot, the existence of successive peaks can be derived, however, with a difference in amplitude as, for example, 100 Ka with a higher frequency and 9.9 Ka with a lower frequency. This is explained by the fact of an existing harmonic relationship between the two figures being in this case 9.9 Ka ~ 10 Ka × 10 = 100 Ka.

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Figure 3. MOC2_148 Mars North polar cap cross section: marking measurement location of the layers in the icy deposits.

Figure 4. Image MOC2_300 showing an upper icy and dust series of layers overlying dark layers with considerable amounts of sand.

Fairbridge reminds to the law of harmonics well known from interplanetary relationships. The measured frequency is put into a preconceived formula spreadsheet, called NewARtest, in which the reported age of the frequency peaks is calculated. Since the ExSpect cycle computing method is totally different in approach from any other classical modeling, control cases for this method of cycle computation were checked on various series of analogues of time series, which were estimated before by classical modelers using only idealized parameters [12].

2. The ExSpect Methodology Developed on Sediment Series of Mars Even when geodynamic processes on Mars cannot yet be described in full detail, it appears from two recent Mars Orbiter images MOC2_148 (Fig. 3) [13] and MOC2_300 (Fig. 4) [14] selected from the NASA online photo journal that, like on Earth, stratigraphic sequences forthcoming from geodynamic sedimentary processes can be observed. A special parameter was introduced for the computation of time series on these images. 2.1. The Relative Sediment Deposit Genetic Rate Since the age for the sedimentological features on Mars is not known and considering the fact that no lower or upper boundary can clearly be determined, the parameter that is used for application of the ExSpect method on Mars can only be approximate. In order to obtain such a parameter, layers on Mars are to be measured on basis of their relative thickness,

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which is called, here, the relative sediment deposit genetic rate (RSDGR) parameter. Cycle calculation on Mars is then carried out with this parameter. This in contrast to the Earth, where many kinds of parameters—such as NIR spectroscopic weathering indexes, palynological data, sedimentological data, sedimentation rates, C-14 fluxes, and still many others—are available for the calculation of palaeoclimatic cycles. The method will be explained in detail hereafter in commenting measures carried out images MOC2_148 (Fig. 3) and MOC2_300 (Fig. 4). In order to be able to check whether depositional cyclicities on Mars would be similar to the ones on Earth, nine different simulations are made each time: 1. Sun’s orbital precession (SOP) of 178 yr or 178 a. 2. Key resonance (KR), key planetary resonance of 298 yr or 298 a. 3. 12,500 yr, or 12.5 Ka, being the last interglacial (Holocene on Earth), the actual interglacial. 4. 125,000 yr, or 125 Ka, being the last interglacial-glacial cycle on Earth. 5. 400,000 yr, or 400 Ka, being the main desertification and gravel bed cycle on Earth. 6. 1,800,000 yr, or 1.8 Ma, being one of the proposed Tertiary-Quaternary boundary on Earth. 7. 2,200,000 yr, or 2.2 Ma, being the Tertiary-Quaternary boundary on Earth used for ExSpect. 8. 2,400,000 yr, or 2.4 Ma, being the Tertiary-Quaternary boundary on Earth, including the transitional basic Red Soil, which is of latosolic nature all over the world. 9. 4,600,000,000 yr, or 4.6 Ga, being the supposed Age of planet Earth. The first and second of these simulations are of the very short-term period; the third of the short-term period; the fourth and fifth of the middle-term period; the sixth, seventh, and eight of the long-term period. All simulations refer to different climato-stratigraphic cyclicities, as described earlier in the threefold classification by Paepe and Van Overloop for the Quaternary Period (or upper part of the Cenozoic Era) on Earth (Fig. 1). 2.2. ExSpect Applicability on Mars As stated above, two Mars Orbiter Camera images were selected from the NASA online photo-journal for calculation of cyclic frequencies in Mars sediments: MOC2_148 and MOC2_300. They are downloaded in the highest resolution and read into Corel Draw. 2.2.1. Measuring Relative Sediment Deposit Genetic Rate on MOC2_148 Figure 3 shows, in MOC2_148, three sections of North Polar Mars layers consisting of typical graded bedding, inferring a progressive and gradual change in particle size from apparently coarse textures at the base to fine ones at the top for each successive layer. The typical graded-bedding deposition shows a recurrent system that is attesting, once more, the climatic evidence in the sedimentation pattern. Each layer is measured via the guidelines option so that the pixel values are figured out in the guidelines-position box. These values are transmitted into a spreadsheet for further processing by Interpolgeo, ExSpect, and NewARtest. Another important climatic feature occurs due to the presence, located near the middle of the considered sequence, of an apparently cold disturbed load-cast (cryo-turbated) horizon, characterized by a chaplet of drip structures. It is taken as a reference surface since it can be located in all three sections of the recurrent graded-bedded system. This reference surface is taken as a marker horizon in the recurrent sedimentation. In order to obtain the highest resolution, measurements of the sediment thickness for the RSDGR on this photograph are taken in two places: (1) At the lowermost section on the right, under the reference surface, and (2) at the uppermost section on the left, above the reference surface.

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Table 1. Cyclicity calculations for several simulations.

Since no lower or upper sedimentary boundary is observed, time simulations are derived from a number of layers of which neither the age, nor the deposition time-rate is known. Therefore, the double AR is used, as to filter out a general cyclicity trend of external forcing factors, presumably palaeoclimatic periods, which in this case will only yield an approximate age of the deposit. A total of 121 data points could be measured for the RSDGR, indicating the differences in thickness of the stratigraphic layering. After processing the 121 data points indicating the sediment thickness of the RSDGR on Fig. 3, for the above mentioned time spans, following results are obtained from Table 1. Only the cycles corresponding or similar to the palaeoclimatic cycles on Earth are taken into account in order to make the following comparison: • Rounded RSDGR cycles for a 12,500 a simulation—5,000, 2,000, 1,250, and 1,000 a. • Rounded RSDGR cycles for a 125 Ka simulation—60 and 21 Ka and 12,500 a. • Rounded RSDGR cycles for a 400 Ka simulation—206 and 40 Ka. • Rounded RSDGR cycles for a 1.8 Ma simulation—none. • Rounded RSDGR cycles for a 2.2 Ma simulation—107 and 22 Ka. • Rounded RSDGR cycles for a 2.4 Ma simulation—112 and 22 Ka. The main Milankovitch cycle of the insolation (21 Ka), gives an important signal in the 125-Ka simulation and somewhat less accurate in the 2.2- and 2.4-Ma simulation, which corresponds with the Tertiary-Quaternary boundary on Earth, indicating the start of the ice ages on Earth. The obliquity (41 Ka) cycle’s signal is quite strong in the 400-Ka simulation. The eccentricity (100 Ka) cycle’s signal is represented to be the least accurate but is the strongest in the 2.2- and 2.4-Ma and 400-Ka simulations. Very striking is the strong presence of the 60-Ka cycle signal in the 125-Ka simulation. The 60-Ka cycle on Earth is the typical interglacial-glacial cycle on Earth, directly indicating a Last Glacial Oscillation [8]. Moreover, the 125-Ka simulation yields the 12,500 a, which stands for the Current Interglacial (Holocene) on Earth. The 400-Ka desertification

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Figure 5. A threefold picture of ice and dust layers (a) on Mars, ice and dust above sandy periglacial deposits (b) on Mars and ice and dust above sandy periglacial deposits (c) in Antarctica (Roland Paepe).

cycle, being a multiple of the 100-Ka Milankovitch cycle, appears as a multiple frequency peak in both the 2.2- and 2.4-Ma simulations. For the 12,500-a simulation, all cycles determining the stratigraphic and archaeological subdivisions on Earth are obtained. Since these cycles are a direct consequence of planetary and sun activity influence [15], it proves that the same influences play a role on Mars as on Earth and that they are in full resonance with each other. 2.2.2. Measuring Relative Sediment Deposit Genetic Rate on MOC2_300 In order to have precise RSDGR calculations, a section where lower and upper parts can clearly be distinguished, the MOC2_300 image, has been selected (Fig. 4). It was taken by MOC in April 2001, near the Mars polar cap, showing a section of 14.5 km or 9 mi across. It has two types of layers, which were described by the MOC staff as follows: “The lower, dark layers of the polar cap appear to include considerable amounts of sand, while the upper layers lack sand and instead may be a mixture of ice and dust.” This description is extremely general and simple, with no clues as to the origin and nature of the deposits except for the presumed dust and ice in the layers at the top of the sequence. Although it is mentioned that dozens of MOC-images helped to determine the origin of both packages of layers, the comments as reproduced with this single, albeit remarkable image, do not reveal any clear suggestion about the genuine genetic nature of the sediments. Nevertheless, there is a remarkable resemblance with sections of equal length and height observed in bluffs of glacier fronts in the glaciers of the Dry Valleys of Antarctica (Fig. 5). As to the front of the Commonwealth Glacier in Taylor Valley (Photo: R. Paepe, 1970, Dry Valleys, Antarctica in Fig. 5(c)) showing typical movements of terminal protruding ice lobes, the location of the image MOC2_300 in the region of Chasma Boreale (Fig. 5(b)) may strongly suggest a similar position and evolution. As described in 1970 [Paepe], this is probably a similar evolution of glacier ice overriding earlier deposited periglacial sediments—in the vicinity of the glacier. An attempt is hereby made to give a suitable explanation for this similarity of the glacier geomorphs of Earth (Antarctica) and Mars (Chasma Boreale). The question is now raised: To which of the earlier revealed Global Climate Change periodicities on Earth, does the above stated movement of the ice layers in Image MOC2_300 possibly correspond? This immediately brings us to the next question: Is there any direct genetic causal relationship between the darker lower layers and the brighter upper layers of the deposits shown in MOC2_300 (Fig. 6) If one is capable to determine similar (dated) conditions on Earth, this would eventually enable the detection of a kind of resonance between Earth and Mars.

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Figure 6. An attempt for a stratigraphic subdivision of the Chasma Boreale polar ice lobe overriding earlier periglacial deposits of the protruding ice front.

The following description of the beds may clarify our interpretation of the image: •

•

The lower beds consist of a series of cross-bedded units, each composed of rhythmic, layered darker and brighter recurrent strata. On Earth, they are reminiscent of glacial lake deposits built up by glacier melt-waters in front of a progressing glacier lobe. Stages (7) and (6) were initial stages when the glacier lobe was still far off and a regimen of braided river was dominating. Recent erosion shaped new benches in these deposits. Stages (5), (4), (3) and (2) are sections of intermittent aggradational lake phases, each characterized by a darker upper zone, indicating the end and upper surface of each accumulation phase. Stages (5) through (2) are corresponding to cut and fill processes. The uppermost lake series (1) are totally disturbed by structures very similar to those known on Earth as cryoturbation processes in which sub-angular frozen blocks have been locked up, as it also seems to be the case here.

In summary, Mars image MOC2_300 shows a unique series of glacier ice deposits overlying a glacial lake (7, 6) and braided river (5, 4, 3, 2, 1) deposits, which were built up before the overlying glacier ice reached its present position. At the point of contact between the ice and the braided river deposits (1) cryoturbation features were observed. The sediment series, together with the overlying ice, is considered to build up a climatic sequence of an interglacial stage (glacial lake and braided river deposits) followed by a glacial stage (at the arrival of the first glacier ice). Smaller climatic fluctuations are also attested as, at the top of each braided river sediment layer, a dark homogeneous layer appears. This could represent a kind of weathering horizon, perhaps, a humic horizon. These dark surface horizons represent a relatively long interruption in the sedimentation, attesting less wet conditions. Hence it may be concluded from the image analysis that longer and shorter climatic cycles have occurred during the build up of these deposits. The building of this lake sediment series corresponds to stages in which proglacial meltwaters, during a warmer (interglacial) climatic stage, abundantly covered the area in front of the glacier lobe, assembling into glacial lake-reservoirs during at least five subsequent stages. The fact that only the uppermost lake deposits are affected by cryoturbation may attest to the arrival of the cold glacier front creating a permafrost environmental condition in its immediate vicinity at that moment. From now on, the glacier lobe will steadily increase on top of the glacial lake deposits under continuously stronger and colder climatic conditions. A recurrent bedding of darker and brighter layers of generally the same thickness infers quick periodic changes during dominantly cold-dry prevailing climatic conditions. It seems quite evident that a long, cold glacial phase persisted during the build up of this glacier lobe, thus, giving evidence of a Glacial Cycle (ice and dust layers) following on an Interglacial Cycle (darker layers). With

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which possible interglacial-glacial cycle is being dealt? As shown in Fig. 1, interglacialglacial cycles of different orders and times exist on Earth. The problem now is to disentangle which one could eventually be dealt with here. The seven stages of lake deposits with darker surfaces probably attest to periods of standstill or, at least, of periodic interruption in the glacial lake aggradational (erosiondepositional) cycle. This compares again with features encountered on Earth. In particular, it compares with the feature coinciding with the last interglacial stage, which started ~127 ka ago. Indeed, the stratigraphic subdivision of the last interglacial stage on Earth into seven warm climatic sections interfering with short periods of cooler climatic stages is found on a global scale: on land in all climatic belts, in the ice of glaciers and ice-caps (Greenland, Antarctica), and in the deep-sea sediments. The upper layers in this section composed of ice and dust, probably match the ice strata in MOC2_148, thus, connecting both images in a stratigraphic way. From the broad section in MOC2_300, a relevant piece is cut out for magnification. The first magnification is of 7.427 times. Then, for sake of a more accurate on-screen sediment layers measurement, again in pixels, the cut piece is stretched 3 times in height to a final vertical magnification of 22.282 times. The magnification rate does not affect the ExSpect calculations, since these calculations are aimed to indicate forcing cyclicities. The relative thickness remains the same. The Results after applying the ExSpect program on the RSDGR measurements of MOC2_300 (Fig. 7) follow hereafter. They are produced in the left column of Table 2. It shows the calculated cyclicities for the whole section, dark layer part and upper icy layer part included. For the MOC2_300 photograph, two more simulations are executed in order to check whether any small planetary cycle or sun activity cycle would appear. The following results are given as rounded RSDGR cycles for: • • • • • • • •

178 a: SOP—none 298 a: KR—none 12,500-a simulation—5,000, 2,000, 1,250, and 900 a 125-Ka simulation—61 Ka, 21 Ka, 12,500 a, and 9,000 a 400-Ka simulation—215, 40, and 22 Ka 1.8-Ma simulation—none 2.2-Ma simulation—220 and 440 Ka (multiple) 2.4-Ma simulation—401 Ka

The main Milankovitch cycle of the insolation (21 Ka) gives an important signal in the 125-Ka simulation and is somewhat less accurate in the 400-Ka simulation, which corresponds with the great desertifications on Earth, indicating the origin of big gravel beds on Earth together with severe drought. The obliquity (41 Ka) cycle’s signal is quite strong only in the 400 Ka simulation. The eccentricity (100 Ka) cycle’s signal is not calculated, but appears as multiples of the 100-Ka signal in the 400 Ka and in both the 2.2- and 2.4-Ma simulations. Very striking, again, is the strong presence of the 61-Ka cycle signal in the 125-Ka simulation. The 125-Ka simulation yields the 12,500-a cycle, which stands for the current or present interglacial (Holocene) on Earth and the, on Earth, well known 9,000-a cycle being a multiple of the KR. In the Short-Term time series, the 9000-a cycle is also the one obtained for the duration of the development of permafrost at the surface of Mars. For the 12,500-a simulation, all cycles, which determine the stratigraphic and archaeological subdivisions on Earth are again obtained. The very short time span simulations for the SOP and the KR, do not yield any recognizable results, due to the relatively low resolution of the RSDGR sampling when taking into account the whole packet of sediments of which the lower part is less clearly stratified.

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Figure 7. MOC2_300 Mars North Polar Cap indicating measurements for RSDGR calculations [14].

3. Comparison of ExSpect Relative Sediment Deposit Genetic Rate Results of Mars with those of Earth 3.1. Reasons for Correlation Earth and Mars Cycles It is now possible to compare the obtained cyclicities from Mars with those of Earth. Just like the resemblance of geomorphs or bacteria and other indices common to both planets, the fact that cyclicities derived from sediment series from Mars points to cycles of changing global climate just like on Earth would eventually indicate that both planets are, in some respect, in resonance with each other, despite the observed differences as to the state of climatic-environmental evolution and especially as to the degree of evolution of life, which is observed today. 3.2. The Cycles on Earth On Earth, palaeoclimatic cycle calculation (ExSpect) from several geological parameters yielded following cyclicities:

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•

On the basis of the glacial-interglacial geo-soil sequences—comparable to Milankovitch cycles: -

•

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100, 41, and 21 Ka. 31, 62, 13, 11, and 20 Ka. • 51, 35 and 55, 76, 89, and 127 Ka.

On basis of the geo-archaeological fine layered sequences—comparable to the Fairbridge [ ] short astronomical cycles: -

3,183, 1,853, 1,163, 927, 513, and 319 yr. 298 yr (KR or Saturn-Jupiter lap (SJL)). • 220-, 146-, 108-, and 86-yr cycles.

These latter short cycles (derived from number of archaeological sites on Earth and, especially, from Greece where they are best dated and most abundantly displayed) are in round figures (5,000, 2,500, 1,250 and 1,000 yr), controlling the climatic evolution and subdivision of the geological last 10-Ka Holocene Epoch and of the archaeological timescale as well as described by Paepe & Van Overloop [4]. These geo-archaeological cycles are then, for the same reasons as for the natural sediments and the geo-soil cycles, indicative of climatic-environmental cycles to which Man had to adapt his way of life in order to survive. 3.3. The Cycles Obtained on Mars In Section 3.3.1, the before mentioned Earth cyclicities are compared with the cycles obtained from Mars, equally, on the basis ofExSpect results of RSDGR for simulations of MOC2_148 and of the total section (lake deposits and ice cap) of the MOC2_300 image. 3.3.1. The MOC2_148 and MOC2_300 Image Simulations The results for the MOC2_148 simulations are as follows: • • • • • • • •

178-a simulation: SOP—none. 298-a simulation: KR—none. 12,500-a simulation—5,000-, 2,000-, 1,250-, and 900-a cycles. 125-Ka simulation—61 Ka, 21 Ka, 12500 a, 9000 a cycles. 400-Ka simulation—215-, 40-, 22-Ka cycles. 1.8-Ma simulation—none. 2.2-Ma simulation—220- and 440-Ka (multiple) cycles. 2.4-Ma simulation—401-Ka cycle.

The results for the MOC2_300 image simulations are as follows: • • • • • • • •

178-a simulation: SOP—none. 298-a simulation: KR—none. 12,500-a simulation—5,000-, 2,000-, 1,250-, and 900-a cycles. 125-Ka simulation—61-Ka, 21-Ka, 12,500-a, 9,000-a cycles. 400-Ka simulation—215-, 40-, and 22-Ka cycles. 1.8-Ma simulation—none. 2.2-Ma simulation—220- and 440-Ka (multiple) cycles. 2.4-Ma simulation—401-Ka cycle.

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4. Conclusive Remarks 4.1. Conclusions 1 The ExSpect-Spectral analysis method, originally applied on Earth, has been successfully applied on RSDGRs on periglacial deposits of Mars, and show time simulations similar to the quaternary palaeoclimatic cycles on Earth. Similar cyclicity figures for all long (400 Ka, 2.2 and 2,4 Ma), middle (125 Ka) and short (12,500 a and less) terms appear to be combined for Mars and Earth. Therefore, it can be stated that RSDGR forcing agents, such as planetary and Sun activity influence as they determine climatic changes, are in resonance for both planets. 4.2. Conclusions 2 Periglacial Mars deposits in Chasma Boreale are as follows: • •

125-Ka and 12,500-a simulations contain the most accurate periodicity signals—61 and 21 Ka, 12,500, 9,750, 5,000, 2000, 1,250, and 1,000 a. 400-Ka simulation—215 Ka, 40 Ka, 30 Ka, 23 Ka cyclicities.

Milankovitch cycles (100 Ka, 41 Ka and 21 Ka) signals are present in the Mars deposits. Simulations of more than 400 Ka do not show other Earth-known cyclicities The Mars North polar glacier sequence represents the presence of the Last Glacial-Last Interglacial on Mars. 4.3. Conclusions 3 ExSpect results of MOC2_300 total section (periglacial lake deposits and glacier) show: • • • •

Upper part (glacier)—very similar: genesis of both the underlying darker layers and the lighter toned upper layers is exactly the same. Climate forcing agents appear to be identical for Earth and Mars, indicating total resonance regarding to the sedimentological dynamics of climatic change. Global Climate Change on Earth in resonance with a synchronous climatic phenomenon occurring on Mars. Features of melting on Mars should then be looked at as due to an extra-terrestrial warming up of both planets.

References [1] Milankovitch M. Kanon der erdbestrahlung und seine Anwendung auf das Eiszeitproblem. Académie royale serbe, Edition spéciale 1941; 133: 633. [2] Shackleton NJ. An alternative astronomical calibration of the Lower Pleistocene timescale based on ODP Site 677. Trans. of the Roy. Soc. of Edinburgh, Earth Sci.1990; 81: 251–61. [3] Liu TS. Loess and the environment. Beijing: China Ocean Press; 1985. p. 251. [4] Paepe R, Van Overloop E. River and soil cyclicities interfering with sea level changes. In: Paepe R, Fairbridge RW, Jelgersma S, editors. Greenhouse effect, sealevel changes and drought, NATO ASI Series 1990; C: 253–80. [5] Van Overloop E. Geological continental cyclicities based on geosoils in the quaternary system. [PhD thesis]. Uppsala, Sweden: Uppsala Universitet; 1998, 144 p. [6] Van Overloop E, Van Biesen L, Paepe R, Han J, Hus J, Peirlinckx L. Application of spectral analysis in the detection of periodicities in continental geological systems. Acta Geologica Taiwanensis 1990; 29: 103–20.

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[7] Van Overloop E, Van Biesen L. Application of a spectral estimation system for the determination of cyclicities in continental sedimentation processes. Proceedings of the 11th Annual International Geoscience and Remote Sensing Symposium, IGARSS 91; 1991 June 3–6; Helsinki University of Technology; 1991; IV: 2051–6. [8] Van Overloop E, Paepe R, Peirlinckx L, Van Biesen L. The 60 Kyr periodicity in the pleistocene. Workshop on Geological Aspects of Global Change in Continental Environments. Free University of Brussels – VUB. 1995. [9] Paepe R, Mariolakos I, Nassopoulou S, Van Overloop E, Vouloumanos N. Quaternary periodicities of drought in Greece. In: Angelakis AN, Issar AS, editors. Diachronic climate impacts on water resources, NATO ASI Series: Global environmental change 1996; I; 36: 77–110. [10] Paepe R, Van Overloop E. Permafrost Equivalents from Boreal to Tropical Zones. In: R. Paepe and V. Melnikov editors. Permafrost response on economic development, environmental security and natural resources, NATO ASI Series: Environmental security 2001; 2; 76: 151–84. [11] Fairbridge RW. Astronomic chronology of climate change during the last 10,000 years. Lecture at Columbia University and NASA-Goddard Institute for Space Studies, New York, 1994: 6. [12] Van Overloop E., Paepe R, Hoover RB. Computing periodicities in Mars sediment time series. In: Hoover RB, Rozanov AYu, Paepe RR, editors. Instruments, methods, and missions for astrobiology IV, Proc. of SPIE 2001; 4495: 55–68. [13] Malin MC, Edgett KS, Carr M.H, Danielson GE, Davies ME, Hartmann WK, Ingersoll AP, James PB, Masursky H, McEwen AS, Soderblom LA, Thomas P, Veverka J, Caplinger MA, Ravine MA, Soulanille TA, Warren JL. MOC2–148. NASA’s planetary photojournal. http://photojournal.jpl.nasa.gov/: 1999. [14] Malin MC, Edgett KS, Carr M.H, Danielson GE, Davies ME, Hartmann WK, Ingersoll AP, James PB, Masursky H, McEwen AS, Soderblom LA, Thomas P, Veverka J, Caplinger MA, Ravine MA, Soulanille TA, Warren JL. MOC2–300. NASA’s planetary photojournal. http://photojournal.jpl.nasa.gov/: 1999. [15] Paepe RR, Van Overloop ES, Hoover RB. Sediment cycles on Mars in resonance with Earth. ESA’s Publication Division (EPD) 2002; SP–518: 165–8.

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Perspectives in Astrobiology R.B. Hoover et al. (Eds.) IOS Press, 2005 © 2005 IOS Press. All rights reserved.

Landscape, Sediment, Red Soil, Permafrost Geomorph Parallels on Earth and Mars Roland PAEPE and Elfi Van OVERLOOP GEOBOUND INTERNATIONAL Research Center, Doornstraat, 27, B-9550 Herzele, & Free University of Brussels, Belgium Abstract. Morphological comparison of biomorphs in astrobiology is a commonly applied methodology to putative bacterial structures found in meteorites from Mars and other extraterrestrial bodies. Geomorphs, such as landscapes, sediment patterns and sequences, red soils, and permafrost polygonal patterns as surficial features, found on Earth find their perfect equivalents on the images of Mars. Moreover, landscape, sediment, red soil and permafrost analogues show a similar geographical distribution on Mars, and they are perfectly comparable to the distribution displayed on Earth. Since the habitat of life is confined to these surface geomorphs of Earth and Mars, it becomes a complex effort to disentangle whether or not the genesis of these geomorph parallels reflect a common evolution on Mars and Earth. These similarities in the shaping and weathering of the surface crusts of both planets point to comparable processes at some point in time and leave the question of why this common evolution is presumed not to continue today.

Introduction The common nature of the number of physical surface features on Earth and Mars is a most striking aspect when studying images of Mars. They immediately lead to questions concerning a possible similar physical evolution of the land surface of both planets. Like biomorphs, which are the signatures of organic life, these numerous physical features bound to the transformation of the land surface are called geomorphs. Geomorphs are the expression of the physical environmental evolution on any planet’s surface or its uppermost surficial layers. Geomorphs essentially developed under the prevailing sub-aerial exogene processes at a given spot on the planet, and hence, they stand in direct relation to changes of the atmospheric conditions, as well. Endogene factors from the planet’s interior, in particular for Earth, certainly play a role, but here, the sub-aerial processes controlled by the surrounding atmosphere will be the focus. In an attempt to build up a comparative study of such common and observable surface features on Earth and Mars, four basic geomorphs have retained our attention: (1) landscapes, (2) sediments, (3) fossil soils, and (4) permafrost. One of the main factors in the building of these geomorphs is, to a lesser or greater extent, water in all its aspects. Furthermore, a considerable amount of biomorphs, which are currently of interest in astrobiology studies are found in these physical geomorph compounds, and it is very much questioned in which ways these geomorphs may have influenced the habitat of life, the oldest signs of life since 3.7 Ga, and the integrated evolution of multicellular life since the Snowball Earth Stage ~0.6 Ga ago. Finally, in a number of case studies, the understanding

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of the physical processes that controlled the common geomorphs of Earth and Mars will be the focus of an attempt to disentangle the basic question of which stage in of evolution is Mars currently situated, i.e.: before or after Earth?

1. The Habitat of Life on Earth Global climatic changes control both geological evolution and evolution of life on Earth [1]. Growing understanding of the geo-dynamic evolution of land surfaces along with the evolution of bio-diversity brought more insight in the relationship between solid earth and its surrounding atmosphere. Actually, processes of interaction between the solid earth (or lithosphere) and the atmosphere form the basic conditions of the habitat of life. All these processes are essentially located in the thin, active boundary zone, the interface between lithosphere and atmosphere, located at the very rim of Earth’s crust surface. For this reason, it is a suitable premise to state that as Earth’s geological environment changes, the habitat of life changes as well, and a fortiori life on Earth. A thorough knowledge of Earth’s land-surface geomorphs and related geodynamic processes may therefore form a basic element for the understanding of geomorphs on Mars and other planets in space. Geomorphs similar to those on Earth may attest to a similar geodynamic evolution and prevailing conditions as well. The long confusing initial conviction that there was water neither in the atmosphere not the land surface of Mars and that the white polar caps consisted of carbon dioxide was probably a major barrier to the application of this concept of geomorph similarity as a result of water. The purpose of the present contribution will be to put more emphasis on the role of water in the genesis of the Mars land surface as was shown in earlier comparative studies between Mars and Earth since 1999 by Paepe et al. [2–4], i.e.: permafrost, desert, and river development are all land-surface forms that give witness to water activity on Mars. A probable second omission in the study of Mars geomorphs is that despite images on Mars showing physical processes similar to those on Earth they have not yet been integrated in a kind of geo-dynamic system like Mars genetic land-surface classification. Actually, it is generally believed, as advocated by Horneck [5], that from 1.5 Ga to the present little, if anything, has changed on the surface of Mars (with the exception of some episodic flows), thus, leaving an enormous time gap for any further landscape evolution. In preliminary stratigraphic classifications of Mars, there is also no room left for rapid land-surface changes over short periods of time. Instead, it is generally believed that huge amounts of liquid water, which could have altered the surface of Mars, are restricted to greater depths and that at the surface only episodic flows of water may have occurred since its origin. Then, how is the observation of surface (melting) water features now visible on recent images of Mars explained? If the omnipresence of water in the geodynamic processes of the surface of Mars can be revealed by such comparative studies with geomorph parallels or analogues of Earth, then the omnipresence of habitats of life under various conditions and aspects on Mars will also become evident.

2. The Oldest Signs of Life on Earth and the Snowball Earth Stage 2.1. Early Forms of Life The next problem to disentangle is related to the oldest signs of life on Earth. It is known that early Earth had a different environment than today. The geological habitat of early life

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responded subsequently to different geological processes than those in which earthly life is surviving today. Even when Earth was formed ~4.6 Ga ago, water-covered areas only appeared to exist as of 3.7 Ga ago, ~1 Ga later. Referring to M. Schidlowski’s older paper [6] and to a more recent paper by Westall et al. [7] for the vestiges of early evolution of life on Earth, it is assumed that life became well established after 3.7 Ga in the Early Archean (Early Archeozoic) as bacterial mats were dwelling abundantly on shallow water volcanic and related sediment volcanoclastic fabric. These early fossils are found today in layers of chert and seem closely associated with original volcanic hydrothermal activity; however, no cyanobacterial fossils have been identified as such in these deposits. In the greenstone metamorphosed province older than >3.7 Ga, no coetaneous bacterial fossils exist although carbon isotope ratios indicate microbial fractionation in the metasediments. Actually, a reevaluation of the lunar bombardment points, shortening the period to only 4.1–3.9 Ga, may be the reason earlier life survived this bombardment. If a hydrosphere existed ~4.4 Ga, life may have already existed at that very early time. 2.2. Old (Pre-Quaternary) Ice Ages and Snowball Earth In the subsequent Proterozoic until the start of the Palaeozoic, ~600 Ma ago, the oxygen level gradually increases. Ancient continents expand by the process of continental drift. Meanwhile, Ice Ages with polar cap development occur (Fig. 1)—the oldest known is the Huronian Ice Age, ~2.3 Ga—then follow a series about every 275 Ma—the Gnejsø Ice Age, ~1 Ga ago; Sturtian Ice Age, ~750 Ma ago; and Varangian Ice Age, ~650 Ma ago[8]. The Snowball Earth Stage, as claimed by Paul F. Hofman and Daniel P. Schrag [9], would have appeared ~600 Ma ago, which should correspond to the Varangian Ice Age cycle in the time period known as the Neoproterozoic. This date is reminiscent of the period when oxygen was increasing in the atmosphere. During that Ice Age, even the tropics froze over. This happened just before the appearance of all recognizable Phanerozoic plant and animal life on Earth, i.e.: before the Cambrian Explosion. It is believed that the latter was the direct consequence of the Snowball Earth Stage in which –50 ˚C ice was growing a kilometer thick all over the globe—a cosmic snowball hurtling through space for more than 10 Ma. Snowball Earth is believed to be a direct result of the specific geographical drifting position of the continents scattered along the equator at that time. After having lasted for 10 Ma or more, the same authors claim that ice masses, whose thicknesses were measured in kilometers only took 1,000 yr to decay. 2.3. Alternating Cycles of Hot-houses (Climatic Warming up) and Cold-houses (Ice Ages) This long-term trend of periodic recurrent Ice Ages holds on throughout the Palaeozoic, respectively with the Ordovician Ice Age, ~490 Ma ago, and the Permian Ice Age, ~210 Ma ago. They are attested by the presence of many relic, fossil, glacial—so-called tillite— deposits occurring all over the surface of Earth. Alleged tillites were recognized and inventoried on all five continents by Hambrey and Harland [10]. In fact, their presence on all continents contributed to the reconstruction of former continents, such as Suess’ Gondwana [11] and Wegener’s Pangaea [12]. After the Gondwana/Permian Ice Age, the earthly climate is triggered again by the well known strong warming up of the Mesozoic, culminating in the Cretaceous maximum. Life on Earth changed dramatically with the dawn of the Age of Dinosaurs. This extremely warm period coincides with the maximum increase of carbon dioxide in the atmosphere together with high bicarbonate sedimentation rates in the oceans. Just as for the Cambrian life explosion right after the Neoproterozoic Ice Age, the Dinosaur explosion coincides with the earthly hothouse right after the End-Permian Ice Age.

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Figure 1. Pre-Quaternary Ice Ages, occurring every 275 Ma (after Schneider et al., 1984) — the Grouping Varangian / Sturtian Ice Age corresponds with the Snowball Earth Stage.

The long cooling of the Tertiary starts ~65 Ma ago. In the course of this steadily cooling, carbon dioxide in the atmosphere rapidly decays and Dinosaurs disappear to be gradually replaced by mammals culminating with the dawn of Early Man ~7.5 Ma ago. This is the transition from macrofauna to microfauna. After an initial dramatic chute, the climate remains rather stable and warm throughout the Paleocene, the Eocene, and Oligocene until the middle of the Miocene ~15 Ma ago. Thereafter, a steadily plummeting temperature curve is observed throughout the Upper Miocene and Pliocene with ice caps forming at Earth’s poles. Gradually the ultimate Pleistocene Ice Age started to develop from about 2.4 Ma, characterized by frequent cold and warm peaks [13,14]: in total 104 were detected in sea and land records within the last 2.6 Ma and 67 Geo-Soils within the last 2.4 Ma (Fig. 3). This considerably amplified the transition from earthly icehouse to hothouse conditions and vice versa. Rapid climatic changes are witnessed during the Pleistocene Ice Age, especially after the Last Glacial Stage, reaching its maximum ~20,000 yr ago when permafrost extended via the flat lands of the Sahara almost to the present equator as a miniature snowball icing. The global decay of these worldwide permafrost and icecap conditions followed rapidly in the aftermath this miniature snowball icing. The rapid transition from the extreme cold Last Glacial towards the warm Holocene of the last 10,000 yr together with the explo-

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sion of new life-forms is similar, although smaller in intensity, to the Cambrian life explosion after the Neoproterozoic Ice Age and the Dinosaur/Mesozoic life explosion after the Permian/Gondwana Ice Age. Coldhouses and hothouses alternate frequently in the climatic evolution of Earth, each with a considerable impact on life and the habitat of life. Whatever the intensity and frequency of these climate changes, life habitat on Earth was not entirely destroyed, and life survived by adapting itself to new conditions of life.

3. The Common Geomorphs of Earth and Mars: Landscapes, Sediments, Fossil Soils, and Permafrost 3.1. Climate Geomorphology: Understanding the Mosaic Distribution of Geomorphs Processes of landscape formation, sediment deposition, fossil-soil pedogenesis, and permafrost development are intrinsically related to global climate changes. All of these processes, to some extent, reflect the impact of the prevailing atmospheric conditions at a given moment of geologic time on Earth’s surface. In 1982, Julius Büdel labeled, for this reason, landscapes as time-bound climatic units, which became the basic concept of his climatic geomorphology [15] theory, translated into English from the original German title “KlimaGeomorphologie” [16]. Herewith, Büdel was pointing to the unbreakable relationship between prevailing specific atmospheric (climatic) conditions at a specific spot on Earth and the synchronous development of a mosaic of specific geomorphs for each of the spots concerned on Earth’s land surface and for each of the categories concerned—landscapes in geomorphology, sediment (time) series in sedimentology, fossil soils (in a soil catena) in the field of pedogenesis, and different degrees of permafrost (patterned-polygonal ground) in the field of cryology. Each of these processes is thus acting synchronously at a specific geologic time creating a specific geomorph on a specific spot. Finally, the juxtaposition of all of these geomorphs along the land surface of Earth results in the mosaic of geomorph. Different geomorphs can occur one next to the other at the same geologic time depending on the climatic belt to which they belong. The whole variety of geomorphs in the same mosaic belongs to the same prevailing global climate—glacial or interglacial, tropoid or temperate—with the only characteristic variation of its geographical position at the surface of Earth. Each satellite image of Earth, Mars, or any other planet is a snapshot of the mosaic at a given moment. In conclusion, one needs the elements of all the combined geomorphs of a given mosaic to understand the prevailing climatic conditions of a given moment for a planet. This statement is quite fundamental in order to extend the concept of Büdel’s climatic geomorphology to extraterrestrial subjects, such as Mars. Even on Earth, it is not easy to explain climate-landscape inter-relationships as processes of landscape building and soil development or pedogenesis along widely differing areas from the Poles to the Equator, vim: throughout regions of permafrost, temperate, desert, and tropical climatic conditions. Indeed, the complexity of all such factors combined such as the atmospheric, climatic, hydrological, hydrographical, geomorphological, sedimentological, pedological, and geological conditions, is quite high. The most common factor linking all of these different processes is, in fact, the specific shaping of Earth’s surface, under the direct aegis of atmospheric changes giving expression to a specific land soil compound, which can ultimately be classified in a geomorphological classification system. Marine morphology (from the deep sea and the shelves) is therefore not considered here since ocean and sea waters protect that portion of Earth’s surface from direct atmospheric impact.

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Figure 2. The genesis of mixed landscapes and related fossil soils at different stages of the Quaternary in Greece (design by R. Paepe).

3.2. The Concept of Mixed Geomorphs and Global Shifting The second important principle introduced by Büdel is the concept of mixed landscapes. It means that, except for the Sub-Polar and Tropical regions, all other landscapes of Earth are composite and mixed in nature. It means that several different landscaping processes were active through time at the same point of Earth’s surface, thus, reshaping all former original landforms, sediments, soil conditions, and permafrost extensions many times. In short, all of the geomorphs of a given moment get mixed if a sequence through time is followed. In imitation of Büdel’s mixed landscape concept this connotation is extended to mixed geomorphs. The mixed geomorphs show a variety of climatic impacts on the original geomorph that will be explained in the case studies for the four concerned. Paepe et al. [17], following the concept introduced by Büdel, extended the global shifting of landscapes to explain the complexity of mixed landscapes that are observed today within the entire framework of Quaternary Stratigraphy. This should not be confused with the processes of continental drift. Here, it simply deals with periodic changes in extension or shrinkage of the equatorial belt towards the poles along parallels of latitude and vice versa for the polar caps. For example, relicts of tropical red soils of the huge tropoid Middle Miocene belt (~10 Ma ago), extended from the Equator to more than 70˚ N in Lapland and 70˚ S in Antarctica, where they are found as vestiges today. Quite the opposite occurred when the tropoid belt was shrinking to its present position between 10˚ N and 10˚ S, and the Polar Caps and surrounding permafrost region was gaining extension from the Poles in the equatorial direction. All intermediate climatic belts and relevant landscapes followed this trend overriding each other’s older landscapes at different geologic times and under different climatic conditions. Büdel’s concept of mixed landscapes as a result of the four shifting geomorphs— landscapes, sediments, soils, and permafrost—is best illustrated during the multiple, frequent, and rapid climatic changes of the Quaternary. With regard to this, Fig. 2 is a selfexplaining example of the complex evolution through time and space of the four geomorphs under consideration in Greece midway between the Poles and Equator.

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Figure 3. In the Quaternary stratigraphic column three soil/sediment time series occur: Long Term of 100 K cyclicity with major (interglacial) geo-soil-GS breaks; Middle Term of the Last Interglacial/Last Glacial cycle with interstadial soil-IS- breaks; Short Term of the Last 10.000 yr (Holocene) with Holocene soil-HS breaks. All series are correlated with the oxygen isotopic deep-sea (OIS) record.

3.3. The Time Series of Sediment, Soil, and Permafrost Geomorphs All of the foregoing statements simply imply that under given global atmospheric conditions, landscapes and, by extension, all other geomorphs under consideration here— sediments, geo-soils, and permafrost—may shift along Earth’s surface in space and time and write over new landform matrices on top of the original, older ones. This means that according to the latitudinal position of one spot on Earth, different types of landscapes will be produced, one on top of the other, and equally, the degree of the weathering of soils will change and superimposed, through time. Hence, time series of fossil soils of different types of development are built up (Fig. 3) in a stratigraphic column of a sediment series, as well. Along with this climatic evolution through time, geomorphs, especially landscapes, sediments, soils and permafrost regions on Earth, are in permanent geo-dynamic evolution. Under the aegis of equally and constantly changing atmospheric conditions, a great diversity of these geomorphs with inherent fauna and flora have developed throughout the deep

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geologic time. Paleontologists have tried since the middle of the 19th Century to disentangle these environments at each stage of the geologic time in order to reconstruct this evolution in the panoramic palaeogeographic display windows of all the natural science museums. Thus, it should be made clear that the position of a certain geomorphologic type of landscape depends not only on its original geographical position at a given spot, but also on its position in the geologic timescale. Outside the so-called virgin regions, such as the boreal glacial and equatorial tropical regions identified by Büdel, all intermediate landscapes are mixed. The concept as it applies to landscapes, sediments, and soils can be extended to all geomorphs as relict evidences of the changing climate through time. They will all be labeled as mixed geomorphs. The multiplicity of Earth landscapes mainly results from the cut and fill process through time. It leads to a diversity reflected not only in the landscape morphology but in the soil-permafrost-sediment sequences of constructional deposits as well. These sequences have built up soil/sediment time series through geologic time suitable for stratigraphic and cyclicity studies.

4. Capita Selecta of Geomorph Parallels Since it is impossible to consider all varieties of geomorphs in this brief NATO-ASI outline, a selection of case studies is provided to eventually detect possible geomorph parallels between Earth and Mars. These capita selecta are: • • • •

Red soils of Earth and Mars. Permafrost on Earth and Mars. Deserts and pediplains. Soil and sediment sequences.

4.1. Red Soils on Landscapes and Sediments of Earth and Mars Referring again to Fig. 3, landscape sequences and related fossil soils on Earth are the most common combination of geomorphs. Both can be followed without interruption from the Middle Miocene to the present in the stratigraphic column (Fig. 3). The geomorphic form of the landscapes is then the result of typical processes of erosion (shaping) and sedimentation (aggradation) acting in close harmony with water activity under the prevailing palaeoclimactic conditions of that moment. On both erosional and aggradational structures, fossil soils are formed and impregnated in the so-called pedosphere (Fig. 4), the thin interphase between the lithosphere and the atmosphere formed under the aegis of the biosphere at a particular moment. Fossil soils essentially register atmospheric conditions of the past as well as the vegetation cover under which they developed. Without vegetation cover, there is absolutely no soil in the pedogenetic sense. One would only be able to speak of a simple geological weathering horizon under the direct aegis of the atmospheric conditions. No vegetation, means that no organic metabolism and no water is necessarily involved. At this stage, the question can immediately be raised as to whether the red soil of Mars (Fig. 5) is genetically a normally developed soil under a vegetation cover or just a simple weathering/oxidation horizon? This question is extremely crucial and was raised earlier by Paepe et al. [18]. For if the red soil on Mars proves to show the geomorph aspect of a latosol on Earth, then its development under tropical-forest environmental conditions is more evident. Furthermore, its position at the present surface of Mars may infer a geologically recent age as to its development. The forest is then the biomorph changing the surface of the geomorph. The same question can be raised for Earth: Was the Earth once entirely covered by a red soil? The answer is definitely yes. This situation existed at the end of the Miocene, ~10 Ma

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Figure 4. Rio Doce, Brazil: Quaternary Latosol soil development on Early Pleistocene gravel beds. The geosoil is the thin interface between the atmosphere/biosphere and the lithosphere/pedosphere media.

Figure 5. (above) Red surface of Mars: Was Earth in the Middle Miocene, 10 Ma ago, like Mars today? (below) Central African planation surface (Burundi) with Quaternary latosol development and Inselbergs.

ago, when the Earth’s entire surface was prevailing under tropical (tropoid) climatic conditions. Fossil red soils found in Lapland and Antarctica above, respectively, 73˚ N- and Slatitude give witness to this occurrence. It is the same red latosol that also occurs as a fossil or palaeo-soil at the base of the Pliocene-Pleistocene soil-stratigraphic sequence in Fig. 3 and is still found in active development in the narrow zone of the tropical areas between 10˚ N and 10˚ S Latitude. 4.1.1. From Global Tropical Miocene Climate to Quaternary Zoning into Climatic Belts As global tropical climate is decaying after the Miocene, differences in temperature become stronger from the Poles to the Equator—at first, moderately temperate during the Pliocene then becoming steadily colder during the Pleistocene Ice Age. This condition leads to the concept of zoning in climatic belts developed along parallels of latitude from glacial cold permafrost regions to the now reduced tropical equatorial regions (Fig. 6). As a consequence, after the global uniform Miocene tropoid climate withdrew from the Poles to the Equator, relicts of tropical soils and landscapes remained all over Earth’s surface until today. Henceforth, landscape processes are no longer uniformly tropical all over Earth today but differentiate into a sequence of landscapes adapted to the newly prevailing climatic

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Figure 6. Pleistocene zoning into climatic belts.

conditions in each of the latitudinal belts. This is the above mentioned phenomenon described by Büdel as climatic-geomorphologic belts of Earth. It results in a subtle differentiation of landscapes (including red soils and all other geomorphs) over writing the sharply contrasting, formerly uniform red planet Earth of the Miocene along traverses from the Poles to the Equator, which are now in harmony with the locally and newly prevailing atmospheric conditions at a given latitude. 4.1.2. A Mosaic of Geomorphs Landscapes—Sediments, Soils, and Permafrost Regions The above also explains why, along such traverses from the Poles to the Equator, a mosaic of different types of landscapes, sediments, soils, and permafrost areas can coexist on the common surface of Earth in regions as far apart as from the polar permafrost region via the temperate wooded land, to the warm mid-latitudinal desert, and finally, to the tropical region with intensive rain and strong fluvial activity. In fact, satellite images are static snapshots of such land-surface mosaics composed of a series of geomorphs, such as those under study here, i.e.: landscapes, sediments, soils, and permafrost, which developed, at different times under different atmospheric conditions. Land surfaces attesting such a mosaic of geomorphs show, as explained before, a mixed composite compound of all environmental elements inherited from several types of geomorph forms developed under different periods of successive climatic evolutions. With regard to a landscape sensu stricto, thus, being of complex origin, it will be difficult, from one, single, static view of a satellite image, to draw conclusions as to its stage of evolution at the present moment of observation. In other words, given the complexity of a geomorph compound, it will be difficult to determine the stage of evolution of the planet’s surface from only one image. This is very much the case when studying images from Mars that have so many features in common with Earth. Indeed, the present static image of land surfaces represented on Mars images appears to be as composite as the landscape features on Earth. It most probably means that landscape features on Mars are also bound to a complex evolution in time and space, for which reason they can hardly be fully evaluated from one single image at time today. An image, for example, of the permafrost surface from the boreal regions of Mars must therefore be integrated in the totality of geographically bound landscape sequences prevailing in other latitudes and not simply as a single image. Actually, any single Mars image is part of the con-

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Figure 7. Images of permafrost-patterned polygonal ground on Mars land surface (left above and below) and on Earth, Dry Valleys in Antarctica (right above and below). The irregular pattern of both upper images reveals heterogeneous subsoil in hilly terrain; the regular pattern of both lower images reveal homogeneous subsoil on flat terrain.

text of a geographical sequence very similar to the sequences on Earth, called geo-soil traverses from Poles to Equator. In conclusion, the knowledge about the evolution of the Earth’s land surface is of primary importance for the understanding of the four geomorph parallels on Mars as discussed here. 4.2. Permafrost on Earth and Mars It is not the intention here to write a manual on permafrost. Some aspects of permafrost will be illuminated for comparison with strikingly similar patterns on the surface of Mars. Patterned ground geomorphs on Earth are usually considered to be typical of permafrost regions (Fig. 7). Unlike mud-cracks or dry-cracks, according to a binding statement by Laachenbruch [19], they form as thermal contraction wedges on almost all surfaces, flat or hilly, provided the superficial subsoil is saturated with capillary permafrost, water-moist or water-ice stratified layers. These wedges (Fig. 8) briefly called frost wedges or ice wedges (when filled in with ice), indicate that the temperature between two subsequent years never rose above –2 ˚C. The impetus at the start of the thermal polygonal cracking of the subsoil is a sudden drop in temperature to –17 ˚C. From the thin proto-fissure at the start, frost wedges grow at a rate of 1 mm/yr. A wedge opening of 1 m at the top of the geo-petal triangle then suggests a frost-wedge growth over a minimum of 1,000 years. As a result of the steady widening and filling of the growing frost wedges at the boundaries of the polygonal patterns, space inside the polygons reduces and sediment layers turn up from the center against the wedges at the polygonal boundaries (Figs 7 and 8). Double-walled/rimed polygons with upturned shoulders on both sides of each wedge are characteristic patterns, especially of low-centered polygons. Fossil wedges from periglacial areas in Belgium [20] or active wedges from Taylor Valley, Antarctica [21] (Photo’s by R. PAEPE) show identical cross sections. They are clearly developed along the edges of polygon fields in the Antarctic Dry Valleys and on Mars as seen in the images of polygons shown in Fig. 7.

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Figure 8. Frost wedges: (left) a recent (1 Ka) and still active wedge in Lake Fryxell terrace deposits (Antarctica); (middle) fossil wedge of the Last Glacial Maximum (20 Ka) in Last Interglacial marine deposits (Brugge, Belgium), and (right) fossil Ice wedge penetrated by active frost wedge in permafrost region along the River Lena (Siberia).

Figure 9. Two MOC Images of Mars in cross sections along bluffs of canons: (above) frost-wedges developed from Mars’ surface underneath patterned ground polygons covered by wind blown deposits. Wedges secondarily eroded along the scarp building talus cones in the lower part; (below) erosion gullies deeply incised in bluff capped by gravels without polygonal structures.

A cross section is shown on a Mars image along a steep scarp under polygon fields (Fig. 9). Secondary erosion with talus developed at the foot of it, may have taken place hereafter. Some believe they are simply erosion gullies. However, the geometrical display of the reversed triangular, fissure-like wedges is too regular for such origin. Water and only water can lead to such results. These Earth and Mars images are good examples of how permafrost geomorphs deliver an undeniable proof of water in the shallow subsoil of Mars. This was published on repeated occasions since 1999 by Paepe et al. [2,3] before the official NASA statement of (deep) water on Planet Mars was published. In another publication [4], an attempt was made to measure the opening of the frost wedges between the upturned double shoulders. It was concluded that the duration of the wedge development at the surface of Mars lasted for approximately 7 to 10 Ka.

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Without being recovered by other sediments, the process may still be ongoing. Ultimately, it implies that an important climatic change occurred on Mars within the last 10 Ka to which the permafrost geomorphs on the Mars land-surface give witness. The newly deposited (flat lake) sediments came under prevailing new cold conditions enhancing the permafrost geomorphs observed on the images. This demonstrates the importance of studying physical geomorphs on other planets. It also reveals that, just like on Earth, it is not absolutely necessary to dispose of huge amounts of water to encounter habitats of life where at least bacterial life could have been preserved. Permafrost extension on Earth has long been known to have varied periodically, according to changes in the extension of polar ice. The maximum of these extensions was carefully mapped in Europe, north of a line from London to Berlin and further to Moscow and turning to the Northern Ice Sea before reaching the Urals. This has been mapped in North America, reaching much lower latitudes than New York [22]. The furthest possible permafrost observed was at Dibeira, slightly south of the Sudanese-Egyptian Border and dated by Paepe [22] at about the Last Glacial Maximum at 18 Ka when polar ice caps reached their maximum southern extension, along the London-Moscow line described above. It may be questioned here how different were the prevailing conditions of those causing the Snowball Earth situation. However, as a response to this southward broadening of the permafrost region, the tropical forest around the Equatorial Belt disappeared and changed into an arid desert region with dry cracks in the shallow subsoil at the same time stratigraphic position as the frost wedges in the North. The Sahara was, for the most part, under patterned ground conditions while the savannah and even the tropical forest decayed with the exception of some relict forest, e.g.: around Kisangani in Congo. 4.3. Deserts and Pediplains A very striking geomorph similarity also exists between the meseta or table desert landscapes of Earth, such as the famous Nubian Desert, and the meseta desert observed on images of Mars about the same mid-latitudinal position (Fig. 10). The meseta deserts are characterized by the table landform, i.e.: Inselbergs or island mountains. The table-form is a result of differential weathering as explained by King [23]. The flat top consists of a hard ground, resistant to erosion, which in Nubia, is most likely to be formed by a laterite duricrust. The laterite is the end product in the pedogenetic sense of the evolution of the former tropical latosol under a process known as climatic degradation under growing arid conditions. This implies a climatic change from savannah to arid climatic conditions. Before laterization, the latosol area was formed by a long-duration climato-pedologic process, which led to the development of planation surfaces (peneplains). After the degradation of the latosol, the vast region capped by the newly formed laterite may eventually become the subject of a general, however, differential uplift (epeirogenesis). Parts of the laterite area can be covered by newly deposited sediments and hidden from further erosion. Other parts are tilted and affected by block faulting. Here the laterite platform is tilted and dissected into a system of quadrangle compartments bordered by rift valleys. The East African Rift (of which the Nile Valley is its northward extension) is huge one but there are a multitude of smaller rifts surrounding the major rift. After compartmentalization by faulting and vertical erosion of all rifts, the ongoing evolution of aridity, a process of lateral erosion in the rifts, sets in. King [23] called this the free cliff recession process, which results in the pied-de-stalle morphology of the mesa with extremely steep cliffs surrounding the Inselberg on all sides, i.e.: the mesa. The process of parallel free cliff retreat can only occur in dry deserts under the aegis of periodic water transport, a little precipitation every half a century. The second condition is

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Figure 10. Meseta or table-landscape-deserts: (left) on Mars and (right) the Nubian Desert in Sudan.

that there is no vegetation, only desert. Vegetation would hamper, first, the free cliff condition of being permanently exposed to sub-aerial weathering and consolidate the slope debris by pedogenesis, and second, it would hamper the removal of the slope debris due to occasional water transport during the few phases of episodic precipitation and water flow. Devoid of any vegetation cover, water could become a most effective means of transport for the loose sediments piled up against the steep slope. Once the slope is freed from slope debris, new sub-aerial erosion could continue to attack the steep free cliff, crumbling to the foot of the steep slope in the interphases of the long-term precipitation cycle. Each time this process is enhanced, there is a parallel retreat of the steep cliff resulting in the table form of the Inselberg and in broad debris plains or pediplains between the mesas. This, alone, is a process involving water even when it is only needed episodically. This process of parallel free cliff recession, as just described, was adopted in the early 1950s by all geologists working on Pediplains and Peneplains in Africa and in the southern United States. The mesa landscape development reveals two different processes of long duration: (1) under peritropical savannah conditions of Central Africa with latosol peneplanation (Büdel’s double denudation) and (2) after the savannah changed into marginal desert regions like the Nubian Desert, the laterite duricrust formation, and subsequent pediplanation under the aegis of the process of parallel free cliff retreat. Since there is no other region on Earth attesting such a climate-morphological evolution, the pediplanation process may be considered as unique for the meseta landscapes. Hence, it is concluded that meseta landscapes on Mars infer similar arid pediplanation processes under the aegis of episodic water activity after a period of higher humidity and of a possible vegetation cover.

5. Conclusive Remarks Despite the shortness of the instruction given in this summary of the course, there are, nonetheless, a number of important conclusions to be formulated on the basis of the four geomorph studies concerning the habitat and origin of life. These conclusions are: •

The four geomorphs, i.e.: landscapes, sediments, soils, and permafrost, are integrated systems occurring on Earth and Mars.

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•

•

•

The landscapes of Mars provide, as on Earth, a zonal distribution from the Poles to the Equator, each zone corresponding to a specific climatic belt with specific geodynamic processes. There are permafrost regions around the polar caps, dry desert mesetas with interfering pediplains in the mid-latitudinal locations, broad areas of dominantly lake and fluvial deposits, and broad erosion surfaces (peneplains) covered with red soil relicts. This variety of landscapes, even when frozen today, is proposed to have originated from a geodynamic evolution on Mars, similar to that of Earth, causing the morpho-climatic regions, as Büdel described them for Earth. All landscapes, without exception, imply a strong action of water. The red soil covering broad spaces of Mars seems to be similar to the general latosol condition of Earth before the period of the Quaternary/Pleistocene Ice Age Zoning, when the tropoid Miocene climate (>7–10 Ma) was controlling the totality of Earth’s surface. The red cover on Mars is not restricted to areas like hot deserts where only oxidation of the surface under sub-aerial weathering conditions takes place. Therefore, it is believed that the red surface of Mars compares with Earth’s Miocene Tropoid surface (and others during the Dinosaur Age) when Earth was also a red planet. In this respect, it is believed that the red soil surface of Mars could be a latosol surface as well, which compares well with the continuity of the almost complete coverage of the planet, just like Earth at the Middle to End Miocene. Instead of oxidation consuming a lot of oxygen from the atmosphere [1–3], such a latosol soil cover could only be produced under peritropical savannah conditions inferring huge precipitation for at least 6 months of the year. From these statements about the studied geomorphs, there is ample indication that large global climatic cycles once prevailed (and probably still prevail) on Mars, just like on Earth. Indeed, there seem to have been such extreme stages as Snow Ball Earth versus the Tropoid Red Soil weathering, geomorphs attest that all climatic belts of Earth are encountered on Mars, and that small cycles are encountered. With all of these conditions of the physical habitat of life being fulfilled, why did evolution of life on Mars stop?

References [1] Schneider S, Londer R. The coevolution of climate and life. San Francisco: Sierra Club Books; 1984. p. 563. [2] Paepe R, Van Overloop E, Hoover R. Interference or comparison between Mars and terrestrial landscapes as an evidence of water and its cycles. SPIE 1999; 3755: 130–43. [3] Paepe R, Hoover R, and Van Overloop E. Patterned ground as an evidence of water on Mars. In: Paepe R, Melnikov V, editors. Permafrost response on economic development, environmental security and natural resources, NATO ASI Series 2, Environmental Security 2001; 76: 581–8. [4] Paepe R, Van Overloop E, and Hoover R. Permafrost patterns and sedimentological cycles on Mars. ESA’s Publication Division (EPD), Special Publication 2001; SP–496: 239–42. [5] Horneck G. Human missions to Mars and astrobiology: two sides of the same coin. ESA’s Publication Division (EPD), Special Publication 2002; SP–518: 269–73. [6] Schidlowski M. A 3.800 million year isotopic record of life from carbon in sedimentary rocks. Nature 1988; 333: 313–8. [7] Westall F, Nijman W, Brack A, Steele A, Toporski J. The oldest fossil life on Earth, its geological context and life on Mars. ESA’s Publication Division (EPD), Special Publication 2001; SP–496: 81–5. [8] Frakes L. Climates throughout Geologic Times. Amsterdam: Elsevier Publishers; 1979. p. 273. [9] Hoffman PF, Schrag DP. Snowball Earth. Sci. Am. 2000; January: 50–7. [10] Hambrey MJ, Harland WB. Analysis of Pre-Pleistocene glacigenic rocks. In: Schlüchter Ch, editor. Moraines and varves, origin, genesis, classification: proceedings of an INQUA symposium on genesis and lithology of Quaternary deposits, Zurich, September 10–20, 1978. Rotterdam: AA. Balkema; 1979. p. 271–5. [11] Suess E. Das Antlitz der Erde. 1885. 1.

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[12] Wegener A. Die Entstehung der Kontinenteund Ozeane. Braunschweig: Sammlung Vieweg; No. 23; 1915. p. 94. [13] Paepe R, Mariolakos I, Nassopoulou S, Van Overloop E, Vouloumanos N. Quaternary periodicities of drought in Greece. In: Angelakis AN, Issar AS, editors. Diachronic climate impacts on water resources, NATO ASI Series I: Global Environmental Change 1996; 36: 77–110. [14] Paepe R, Van Overloop E. Permafrost Equivalents from Boreal to Tropical Zones. In: Paepe R, Melnikov V, editors. Permafrost response on economic development, environmental security and natural resources, NATO ASI Series 2, Environmental Security 2001; 76: 151–84. [15] Büdel J. Climatic Geomorphology. Princeton: Princeton University Press; 1982. p. 443. [16] Büdel J. Klima-Geomorphologie. Berlin: Gebrüder Bornträger; 1977. p. 304. [17] Paepe R. Landscape changes in Greece as a result of changing climate during the Quaternary. Proc. Info. Symp, EEC Programme Climatology, Mytilene 1984, Special Volume 1986; 49–58. [18] Paepe R, Van Overloop E, Hoover R, Nassopoulou S, Kafumu P, Wang D. Red soils on Earth and their significance for Mars. In: Hoover RB, Rozanov AYu, Paepe RR, editors. Instruments, methods, and missions for astrobiology V, Proc. of SPIE 2003; 4859, 93–107. [19] Lachenbruch AH. Mechanics of thermal contraction cracks and ice-wedge polygons in permafrost. Geol. Soc. Am., Special Paper 1962; 70: 721–52. [20] Paepe R, Vanhoorne R. Eemian Sediments nearby Bruges (Belgian Coastal Plain). Professional Paper, Belgian Geol. Surv. 1972; 9: 29. [21] Paepe R, Paulissen E. Frost wedge forms in relation to their geomorphological and stratigraphical position in Taylor Valley (Antarctica). Professional Paper, Belgian Geol. Surv. 1974: 3: 26. [22] Paepe R, Van Overloop ES, Hoover RB. Comparison of Snowball Earth and Mars conditions. In: Hoover RB, Rozanov AYu, Paepe RR, editors. Instruments, methods, and missions for astrobiology IV, Proc. of SPIE 2002; 4495: 40–54. [23] King LC. Cañons of landscape evolution. Bull. Geol. Soc. Am. 1953; 64: 721–52.

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Biochemical Markers in Rock Coatings Randall S. PERRYa and Vera M. KOLBb Department of Earth and Space Science University of Washington, Seattle WA 98195–1310, USA b Department of Chemistry University of Wisconsin-Parkside, Kenosha, WI 53141–2000, USA a

Abstract. Rock coatings are ubiquitous in arid regions of the world. Amino acids in desert varnish coatings have been measured, and other organic compounds have been considered as chemical biosignatures in coatings. Understanding the mechanisms of formation or rock coatings and identifying their active and fossil biosignatures will provide useful methods for contrasting biotic and abiotic systems on Earth and other planetary bodies.

Rock coatings are ubiquitous in arid regions of the world [1–3]. It is suspected that rock coatings may also exist on Mars, as suggested by observations of both the Viking and Mars Pathfinder landing sites [4]. One of NASA’s goals is to look for the biosignatures of those coatings [4]. In addition, NASA is interested in furthering the general knowledge of the chemical signatures of bacterial fossils to facilitate the observation of their possible presence in meteorites, especially those from Mars [5,6]. First, there will be a brief background on various rock coatings, including desert varnish, and then a discussion of biofilms and microbial relationships to desert varnishes. Then, the biosignature issue, including the most current results and rationale for the expansion of biosignatures to include saccharides, will be addressed. Rocks on Earth weather and change through time, and microbes play an important role in this process [7–9]. This role may either be an active one in forming minerals, e.g.: the formation of magnetite in microfossils [5], or it may be a passive role, e.g.: a change in redox conditions, the by-products of metabolic processes, pH changes, or the complexing of ions by exopolymeric substances (EPS). Rocks also become coated with minerals (Figs 1–4) that may protect them from weathering, and microbes may form or contribute to the formation of the coatings. Bacterial, Archaean, and fungal cell walls and their associated EPS and spores, interact with mineral surfaces and ions; microbes eventually die, and all of their substances, composed of both living and dead cells are reprocessed and may become part of rock coatings and biominerals, such as forsterite or opal [10]. Desert varnish, also called rock varnish, is found in deserts and semi-arid regions throughout the world. They are coatings, not weathering products of the substrate (Fig. 4), composed principally of clays, oxides, hydroxides, manganese, and iron. The bulk inorganic chemistry has been well characterized [3,11,12]. Previously, organic compounds had been thought to be only a small component of varnishes [1,13]. Most electron microprobe data have shown 80–90% weight oxides, and it has been reported by Perry [14] that the water content is close to 10%. However, only a few samples of varnish were analyzed for their water content, and they may have been composed of uncharacteristically hydrated clays. Organic compounds may comprise the material that was unaccounted for, as sup-

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Figure 1. Surface texture of varnish. Detrital grain in upper right quadrant (scale bar is 2 µm).

Figure 2. Surface texture of varnish ×1,000. Uncoated rock substrate left and right (scale bar is 20 µm).

Figure 3. Microcolonial fungus on varnished rock.

Figure 4. Thin section (10 µm) of desert varnish.

ported by Nagy et al. [13] and Perry et al. [15], whose studies indicated that there is a measurable biogenic, organic component to rock varnish and that the organic components can possibly be used as chemical markers for coatings. Biofilms are composed of EPS and microbes and are ubiquitous even in arid conditions. They can be highly hydrated in aqueous environments. However, biofilms on exposed rocks may have as little as 1% water [16]. Subaerial biofilms on natural surfaces collect detrital grains in their slime and complex metals [17]. EPS and cell components may contain many chelation sites, which are implicated in mineralization processes [17]. Individual microbes rarely come directly into contact with minerals but rather attach to surfaces with extracellular polymers [18,19]. Desert varnish presents botryoidal (Figs 1 and 2) or in ultra-thin sections of ~10 µm [12] wavy lamina (Fig. 4). In thin section, biofilms also consist of finely repetitive layers that are wavy and discontinuous. Even with the severe conditions in deserts, where temperatures reach over 60 ˚C and frequently reach 80 ˚C on the dark varnish surfaces, EPS and biofilms along with complexed metals might be preserved or incorporated into varnish coats. Biofilms are almost ubiquitous where there is a substrate interface and a liquid, and since water is available even in extreme arid conditions, desert varnish can be realistically described as a subaerial biofilm.

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There is ample evidence for associations of microbes with varnish-coated rocks. Many have suggested that varnish formation may be microbially mediated [2,15,20–26]. Hungate et al. [25] isolated 79 strains of bacteria from varnish coatings from the Negev Desert. Seventy-four of the bacteria could oxidize manganese, and all but one were gram-positive. As noted by Staley et al. [2], most of the bacteria isolated from varnish are gram-positive organisms. Bacillus subtilis was cultured from varnish from the Deem Hills area north of Phoenix, AZ [12]. A study by Palmer et al. [27] found that most of the isolates from the Sonoran and Mojave deserts capable of manganese oxidation were gram-positive bacteria, including Micrococcus, Planococcus, Arthrobacter, Geodermatophilus, and Bacillus. Eppard et al. [28] found only members of the order actinomycetes, including the Geodermatophilus species, on rocks and monuments with the exception of one Bacillus. In addition to bacteria, fungus may play a role in varnish formation. Rock varnishes frequently have associated colonies (Fig. 1) of microcolonial fungus (MCF) [14]. Some evidence implicates the involvement of MCFs in desert varnish formation [24,29,30]. As bacteria on desert varnishes expire, their representative amino acids could become part of the varnish coating and, then, possibly, be used as biosignatures. Perry et al. [15] found D-alanine and D-glutamic acid in the hydrolyzates of desert varnish from the Sonoran and Mojave deserts. Two other non-protein amino acids that were also found are βalanine and γ-amino butyric acid (ABA). D-aspartic acid was also present. The discovery of this D-amino acid is consistent with the report by Nagy et al. [13] who found this compound as the sole D-enantiomer in their investigation of varnish coatings. Finding the Denantiomers of glutamic acid and alanine suggests that peptidoglycan is a component of desert varnish. Peptidoglycans are present in large quantities in gram-positive bacteria and only in very small quantities in gram-negative bacteria. In addition, lysine—found in grampositive bacterial peptidoglycans—was present, and diaminopimelic—found in gramnegative bacterial peptidoglycans—was absent. The amino acid evidence is suggestive of a bacterial biosignature presence in varnish coatings and possibly gram-positive bacteria similar to those that have been cultured from the surface [2,20–26] of varnishes. Another possible candidate for a biosignature within peptidoglycans would be the peptide interbridge composed of five glycines, which is found in some gram-positive bacteria. DNA studies of 16S rRNA and 18S rRNA have produced, as yet unquantified, measurable amounts of DNA in varnishes [31]. The use of melanin as biomarker from MCF colonies from desert varnishes is planned. Since fragments of peptidoglycans have been recovered from desert varnishes, a question was posed: Could other peptidoglycan components also be recovered, and could they be used as additional biosignatures? Peptidoglycans are complex polysaccharides found in bacterial cell walls. They contain linear polymers of two alternating sugars, Nacetylglucosamine and N-acetylmuramic acid, which are cross-linked with the short peptides. These peptides are composed of some common amino acids as well as some unusual ones, such as D-glutamic acid, diaminopimelic acid, and D-alanine [15]. The peptide crosslinks in the peptidoglycans may protect the sugars from decomposition, enabling them to serve as biomarkers. It is currently unknown if polysaccharides or their transforms exist in varnish coatings. In general, sugars have not been studied as a biosignature. There is ample reason for this. Common sugars, such as glucose, ribose, arabinose, or fructose, contain aldehyde or keto groups in conjunction with hydroxyl groups that make them very chemically sensitive. Such sugars are rapidly destroyed under the basic conditions. They isomerize under both acidic and basic conditions. Isomerization causes racemization of the optically active centers and the eventual destruction of the molecules [32], thus preventing their use as biomarkers. However, some sugar derivatives that are devoid of aldehyde and keto groups, notably sugar-related acids and alcohols, are more stable and have been isolated from the

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Murchison meteorite [33]. Sugars may be more stable under arid conditions, where most common rock varnishes are formed. Sugars in general make a variety of stable complexes with metals, such as calcium, aluminum, iron, and manganese [34], that are commonly found on natural surfaces and soils. Such complexes may further protect sugars against destruction. The most likely part of bacteria to interact with rocks is the outer part of the cell wall that contains oligosaccharides from peptidoglycans and other saccharides, such as teichoic acids and related sugar-lipids. Bacteria, on attachment to the surface, also produce adhesive substances that are predominantly polysaccharides. It is likely that bacterial polysaccharides will interact with natural surfaces in a process that is probably facilitated by their initial complexation with metals that are found on these surfaces. The complexation may be followed in some cases by a redox-type reaction. It is known that peptidoglycans are highly interactive with dissolved metal ions [35]. An additional pathway could be via complexation with silicates [36]. Many chemicals have been investigated as possible biomarkers for microbes, such as hopanoids and chiral amino acids [37]. It is hope that additional biomarkers will be added in this study of rock coatings, specifically, polysaccharide components from peptidoglycans, from which unusual amino acids have already been isolated as biomarkers. A simultaneous finding of these unusual amino acids, and the peptidoglycan polysaccharides or their transforms, could indicate the remnants of bacteria cell walls. This would be of importance in the identification of bacterial fossils. Another possible biomarker is dipicolinic acid (DPA) (pyridine-2,6-dicarboxylic acid), which is specific to bacterial spore coats [38]. Spores concentrate ions, such as those of manganese and calcium, in their coats. These may become incorporated in varnishes, and DPA might remain stable in the coating. With new technologies for better microanalyses, the possibilities for identifying additional biosignatures seem imminently achievable. Perhaps, new questions also need to be asked. Because desert varnish is a coating that can form in extreme environments, is a chemical process, and may be microbially mediated, it provides a unique opportunity for testing our ability to understand and interpret biochemical signatures on Earth before attempting to understand their possible existence on other planetary bodies [39–41].

Acknowledgements This research was made possible by a grant from the National Science Foundation, Integrative Graduate Education and Research Training (IGERT) Grant Number DGE–9870713. A portion of the research was performed at the Environmental Molecular Sciences Laboratory, D.O.E., Pacific Northwest National Laboratory, Richland, WA. Thanks are expressed to Michael H. Engel, James T. Staley, and John Adams for their time and advice, and Karin Stewart-Perry for reviewing the manuscript.

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The Influence of Space Parameters like Solar Ultraviolet Radiation on the Survival of Microorganisms Petra RETTBERG German Aerospace Center (DLR e.V.), Linder Höhe, D-51147 Köln, Germany Abstract. At the beginning of biological evolution before a protective ozone layer had developed in the atmosphere, high intensities of energy-rich solar ultraviolet (UV) radiation could reach Earth’s surface. Today, the full spectrum of solar UV radiation is only experienced in space, where other important space parameters, such as vacuum, cosmic radiation, temperature extremes, and microgravity, influence survival and genetic stability. To reach a better understanding of the processes leading to the origin, evolution, and distribution of life on Earth, several in-space experiments have been performed with microorganisms. The ability of resistant life forms, such as bacterial spores, to survive high doses of extraterrestrial solar UV— alone or in combination with other space parameters, e.g.: vacuum—was investigated. The protective effects of organic as well as inorganic substances, such as artificial or real meteorite material, were determined in satellite experiments, on the Space Shuttle, and on the MIR station. It could be shown that thin layers of inorganic material are able to protect spores against the deleterious effects of the energyrich UV radiation and that they are able to survive under these conditions for very long periods of time in space. With different cut-off filters, the effect of an increasing atmospheric ozone layer on the solar spectrum was simulated as it had occurred on Earth ~2 Ga ago, and the resulting changes in the DNA damage inducing potential of solar UV radiation was investigated. Extraterrestrial solar UV radiation was found to have a thousand times higher biological effectiveness than UV radiation filtered by stratospheric ozone concentrations found today on Earth.

Introduction On Earth, solar UV radiation has had a strong impact on the early evolution of life. From model calculations, it can be assumed that during the Archaen era, during which the diversification of early anaerobes took place and the first anaerobic photosynthetic bacteria appeared (~3.5 Ga ago), the amount of free oxygen in the atmosphere was significantly lower than today [1]. There was no, or very little, absorption of solar UV radiation by ozone. Therefore energy-rich UV radiation of short wavelengths could reach Earth’s surface. In all organisms, UV radiation causes temporary or permanent alterations, which result from photochemical reactions with different biological target molecules. The most important one is DNA because of its unique role as genetic material and its high UV sensitivity, with an absorption maximum of ~260 nm. The significance of solar UV radiation as an evolutionary driving force is reflected by the development of different protection mechanisms against the deleterious biological effects of UV radiation, especially by the development of several partly redundant enzymatic pathways for the repair of UV induced DNA damage very early in evolution [2].

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In space, the environmental conditions, e.g.: vacuum, low temperatures, UV radiation, ionizing radiation, and microgravity, are extreme from the point of view of an organism adapted to conditions on Earth. The extraterrestrial solar spectrum extends far into the short wavelengths of UV-C (190–280 nm) and vacuum UV (<190 nm). From laboratory experiments, it can be assumed that, among the parameters of space, solar UV radiation is the most deleterious in killing highly resistant terrestrial organisms, such as bacterial spores. It could be shown that the simultaneous action of energy-rich UV radiation and vacuum even increased the UV sensitivity [3]. Photoproducts in DNA that are difficult to repair enzymatically, such as DNA protein cross-links and DNA strand breaks, were among the most severe injuries produced by UV radiation in the spores while in vacuum. In several in-space experiments, the ability of spores of Bacillus (B.) subtilis to survive high doses of extraterrestrial solar UV alone or in combination with other space parameters, e.g.: vacuum, was investigated. The protective effects of organic as well as inorganic, such as artificial or real meteorite material, were determined in satellite experiments, on the Space Shuttle, and on the MIR station.

1. Determination of the Biological Effectiveness of Extraterrestrial UV Solar Radiation The measurement and assessment of the biological effects of UV radiation require methods that take the strong wavelength dependence of all UV effects into account. DLR-Biofilms are biological UV dosimeters that consist of immobilized bacterial spores of B. subtilis as UV targets and that directly weight the incident UV radiation according to its biological efficiency [4]. In the experiment, SURVIVAL II, on the exposure facility, BIOPAN [5], the biological effectiveness of extraterrestrial solar radiation was determined with the DLR-Biofilm technique on a non-stabilized satellite in Earth orbit (FOTON 9 mission, June 14–30, 1994). One DLR-Biofilm was exposed to the entire solar spectrum. To enlarge the dynamic range of the biofilm dosimeter, it was only covered by four different neutral density filters. The exposure was performed by opening a shutter system connected to a timer for 10 s. A second DLR-Biofilm on BIOPAN remained unexposed as dark control to exclude the possible influence of experimental parameters in space other than UV radiation. After postflight calibration and development, the DLR-Biofilms were analyzed together with a ground-control DLR-Biofilm, which was exposed to the terrestrial solar spectrum in Köln on August 6, 1993 under clear sky conditions. In space, a biologically effective dose of 63 Jeff m–2 was obtained in 10 s (Fig. 1), whereas on Earth, 1 Jeff m–2 was measured in 2.6 min of solar exposure (data not shown). Hence, it can be concluded that the extraterrestrial solar radiation has a biological effectiveness that is ~1,000 times (exactly 984 times in this experiment) higher than the terrestrial solar radiation [6].

2. Estimation of the Potential Effects of Changing Stratospheric Ozone Concentrations by Simulation in Space During the German Spacelab Mission D–2 (April 26–May 6, 1993), in the RD-UVRAD experiment, DLR-Biofilms were exposed for defined intervals to extraterrestrial solar radiation filtered through an optical filtering system with a shutter mechanism. The filter combinations consisted of neutral density filters to enlarge the dynamic range of the DLR-Biofilm dosimeter and of short-wavelength cut-off filters (combinations of Schott filters: WG305

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Figure 1. Determination of the biologically effective dose of a 10 s exposure to extraterrestrial solar radiation by use of different neutral density filters on BIOPAN I.

(1 mm) + WG301 (5 mm), WG295 (7 mm), WG305 (2 mm) + WG320 (1 mm), WG305 (1 mm) + WG320 (1 mm), WG320 (1 mm), WG305 (2 mm) + WG305 (5 mm)) to simulate different ozone column thicknesses from 66 to 440 Dobson units (DU) in the stratosphere. The results of the biological UV dosimetry (Fig. 2) indicate that there is a strong increase in biological effectiveness by decreasing ozone concentrations and, again, that the unfiltered extraterrestrial solar radiation has a biological effectiveness nearly 3 orders of magnitude higher than the values on the Earth’s surface at normal ozone concentration [7,8].

3. Quantification of the Protective Effect of Meteorite Material Against Extraterrestrial Solar UV Radiation Since the discovery of Martian meteorites [9], it has been known that rock fragments can be ejected from planets, e.g.: large meteorite impacts, and that interplanetary transfer of matter has occurred several times in our solar system’s past [10]. Whether living matter can be transported between planets by the same mechanism, and if so, whether resistant organisms can survive this process, are still open questions. In the EXOBIOLOGIE experiment, spores of B. subtilis were used to investigate whether meteorite material offers enough protection for bacterial spores to survive a longterm stay in space. Spores were embedded in real and artificial meteorite material and exposed to space. Four different types of powdered protective material were tested: three were meteorite samples from Murchison, Millbillillie, and Zagami, and as a terrestrial control, a sample of clay from Adendorf, Germany was also tested. The protective material (2.5% w/v) was mixed with the spore suspension (3×109 ml–1) and dried directly on the UV radiation-transparent MgF2 windows of the sample carriers in 20 μl aliquots. As a control, the three following identical sets of samples were prepared in parallel: (1) a laboratory control, which was kept in the dark under 1 atm of air at room tempera-

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Figure 2. Biologically effective solar irradiance, Eeff (254), for different ozone column thicknesses (circles) determined experimentally with the biofilm technique in the D–2 space experiment under a simulated ozone layer of different thickness (triangle, ground control). The solid line without symbols shows the corresponding curve for DNA damage estimated under the assumption of a radiation amplification factor (RAF) of 2. Insert: Biologically effective irradiation, Heff (254), after 3,240 s insolation, measured in space under different ND filters for a simulated ozone concentration (440 DU).

ture, (2) a ground control, kept in the dark under 1 atm of air, which was transported with the flight samples to the sample accommodation and back, and (3) a flight dark control, which was mounted in the lower layer of sample carriers of the flight hardware. The samples of the EXOBIOLOGIE experiment were exposed to space outside the MIR station in the temperature-controlled flight hardware from CNES from April 16 to July 23, 1999. They were irradiated with the full extraterrestrial solar UV spectrum. After retrieval, in each sample, the fraction of viable spores and the number of mutants were determined by resuspension, dilution, and incubation on appropriate nutrient agar plates as described elsewhere [11]. The results of the survival measurements are shown in Fig. 3 for B. subtilis spores of the DNA-repair proficient wild type strain HA101. After exposure to space, ~100% of the spores survived if protected against solar UV radiation, as can be seen from the comparison of the results for the flight dark controls and the ground controls. Approximately 10–4% of the spores survived if also exposed to solar UV radiation. Neither additional significant protection by the meteorite material nor significant differences between the protective materials could be found. The results for the mutations induced during the experiment are shown in Fig. 4. Due to the very low numbers of survivors in the UV-exposed samples (see above), no mutants could be determined in these samples. Figure 4(b) shows the mutation induction factor, defined as the ratio of mutants per survivor of the flight dark controls to the corresponding ground control samples describing the effects of the space environment except UV radiation, mainly the effect of vacuum. In the flight dark controls, the number of mutants was significantly higher than in the ground control samples.

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Figure 3. Averaged number of survivors (N) of B. subtilis spores, strain HA101, mixed with different protective materials (a. dest. = aqua dest., no protective material).

Figure 4. (a) Averaged number of mutants per survivor of B. subtilis spores, strain HA101, mixed with different protective materials (a. dest. = aqua dest., no protective material) and (b) mutation induction factors.

The lowest induction (induction factor of ~1, which is no induction) was found in the presence of a powdered aliquot of Zagami as protectant. The highest induction was found in the samples that contained a powdered aliquot from Millbillillie (induction factor of ~25). Comparable results were obtained from analogous samples with spores of the DNArepair deficient B. subtilis strain TKJ6312 (data not shown) [12].

4. Conclusions Bacterial spores as a model system for highly resistant microorganisms are able to withstand the hostile environmental conditions in space if they are protected against the most

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damaging factor under these conditions, the energy-rich extraterrestrial solar UV radiation. In two space experiments, it could be shown that the biological efficiency of solar UV radiation in space is ~1,000 times higher than on Earth today. The molecular strategies by which B. subtilis spores are able to protect their integrity, especially those of the DNA, against UV-induced DNA-photodamages, vacuum damage, and the damages induced by other space parameters are not yet fully understood and require further laboratory and space experiments. The results of the EXOBIOLOGIE experiment are in accordance with theoretical considerations and calculations of the possibility and probability of a natural transfer of microorganisms through space, e.g.: from Mars to Earth [13]. Real or artificial meteorite material, however, did not protect the spores significantly, but layers of spores inactivated by UV radiation can serve as a UV shield by themselves. A hypothetical interplanetary transfer of life by the transport of microorganisms inside rocks through the solar system cannot be excluded but requires the shielding of a substantial mass of inorganic substances.

References [1] Rothschild LJ, Cockell CS. Radiation: microbial evolution, ecology, and relevance to Mars missions. Mut. Res. 1999; 430: 281. [2] Eisen J, Hanawalt P. A phylogenomic study of DNA repair genes, proteins, and processes. Mut. Res. 1999; 435: 171. [3] Horneck G, Rettberg P, Reitz G, Wehner J, Eschweiler U, Strauch K, Panitz C, Starke V, BaumstarkKhan C. Protection of bacterial spores in space, a contribution to the discussion on Panspermia. Orig. of Life 2001; 31: 527. [4] Rettberg P. The biological UV dosimeter ‘biofilm’. In: Rettberg P, Baumstark-Khan C, Horneck G, Amanatidis G, editors. Biological UV dosimetry, a tool for assessing the impacts of UV radiation on health and ecosystems. Luxembourg: European Communities, Office for Official Publications of the European Communities; 1999. 192 p. [5] Burger F. Biopan—a multi-purpose exposure facility for space research. In: Proceedings of the Sixth European Space Mechanisms and Technology Symposium. Zürich, October 4–6, 1995; ESA SP– 374: 313. [6] Rettberg P, Horneck G. Biologically weighted measurement of UV radiation in space and on Earth with the biofilm technique. Adv. Space Res. 2000; 26: 2005. [7] Horneck G, Rettberg P, Rabbow E, Strauch W, Seckmeyer G, Facius R, Reitz G, Strauch K, Schott J-U. Biological dosimetry of solar radiation for different simulated ozone column thicknesses. J. Photochem. Photobiol. B: Biol. 1996; 32: 189. [8] Rettberg P, Horneck G, Strauch W, Facius R, Seckmeyer G. Simulation of planetary UV radiation climate on the example of the early Earth. Adv. Space Res. 1998; 22: 335. [9] Wasson JT, Wetherill GW. Dynamical, chemical and isotopic evidence regarding the formation locations of asteroids and meteorites. In: Gehrels T, editor. Asteroids. Tucson: University of Arizona Press; 1979. 926 p. [10] O’Keefe JD, Ahrens TJ. Oblique impact: a process for obtaining meteorite samples from other planets. Science 1986; 234: 346. [11] Baltschukat K, Horneck G. Responses to accelerated heavy ions of spores of Bacillus subtilis of different repair capacity. Radiat. Environ. Biophys. 1991; 30: 87. [12] Rettberg P, Eschweiler U, Strauch K, Reitz G, Horneck G, Wänke H, Brack A, Barbier B. Survival of microorganisms in space protected by meteorite material: results of the experiment EXOBIOLOGIE of the PERSEUS mission. Adv. Space Res. 2002; 30: 1539. [13] Mileikowsky C, Cucinotta FA, Wilson JW, Gladman B, Horneck G, Lindegren L, Melosh HJ, Rickman H, Valtonen M, Zheng JQ. Natural transfer of viable microbes in space. part 1: from Mars to Earth and Earth to Mars. Icarus 2000; 145: 391.

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Bacterial Paleontology A.Yu. ROZANOV Paleontological Institute RAS, Profsoyuznaya 123, Moscow, 117997, Russia Abstract. Bacterial paleontology is rather young branch of paleontological studies. Bacteria and microbes in general could be perfectly preserved as fossils. The major part of the sedimentary rocks formed in the photic zone of epicontinental basins of the past originated under the influence of microorganisms. Studies have increased the number of minerals known to be formed with the participation of microorganisms to >100. Bacterial-paleontological data accompanied by the data on the first origin of eukaryotes, metazoans, etc. significantly enrich the knowledge of evolution of the biosphere and reveal a long period of transitional biosphere prior to the appearance of the typical eukaryotic biosphere of the modern type. The bacterialpaleontological data on carbonaceus chondrites make a foundation for the possibility of the presence of extraterrestrial bacterial life.

The important role of bacteria and other microbes in geological processes was suggested long ago. Already, by the end of the 19th century, N.I. Andrusov, in his lectures, spoke about the bacterial role in the origin of some Cenozoic deposits of iron and sulfur. Later, numerous microscopic studies were aimed to prove the presence of fossilized bacteria in rocks. One of the most prominent achievements of that period was A.G. Vologdin’s report [1]. However, the images obtained by specialists using relatively low magnification could not convince the scientific community. Moreover, many specialists of that period who claimed the tremendous role of bacteria in the formation of the sedimentary mineral resources, such as bauxite, iron ores, etc., incurred fierce criticism or even derision by the leading scientists of the period. The significant breakthrough of the post-war science was the discovery of fossil microorganisms in cherts. The pioneering work in this field belongs to Barghoorn and Tyier [2]. Subsequent studies were developed in a variety of countries [3–8]. Vast amounts of material have been collected, permitting the reconstruction of, not only the origin and development of microorganisms on Earth [6,9,10], but also the general pattern of biosphere evolution in the Precambrian. These studies also considered the data obtained by the traditional method of maceration commonly used for extraction of acritarchs, spores, and pollen. In such cases, primarily, forms with organic (acid resistant) shells were extracted. However, the most significant breakthrough was made after the introduction of electron microscopy to the study of microbial remains. The new technology revealed that almost all sedimentary rocks contain well-preserved fossils of bacteria [11–19]. The perfect preservation could not be ensured without high rates of fossilization [12,13,15,20–23], and this result was proven experimentally. The intensive study of fossil bacteria, bacterial paleontology [15], was undertaken during the last decade. On one hand, it is tightly connected with the extensive investigation in

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the field of geomicrobiology, which studies the interrelation of recent microbial biota with rocks, minerals and other materials [24,25]. On the other hand, it is greatly influenced by the study of cyanobacterial mats (CBM), both recent and fossil [13,26,27]. These studies confirmed the extreme antiquity of CBM and their highly important role in the formation of an oxygenic atmosphere and the whole biosphere in general. The significance of the studies of bacteria in extreme environments should be mentioned here. Perhaps, some of those conditions are similar to those present in the Archean. The main task for bacterial paleontology is to study the fossil microbes. Traditional paleontology deals with remains of ancient organisms. It creates systematics based on the organisms’ morphological features considering their phylogenetic relations. The main fields of study that utilize paleontology are evolutionary theory, history of the organic world, and biostratigraphy. Recently, paleontology has yielded priceless data for the study of biosphere evolution. Paleogeography also gains a significant benefit from paleontology. At first, bacterial paleontology is limited in its input data by the simplicity of the objects’ morphology and specificity in systematization of the bacterial material. So, the morphological approach is important, but there is not enough criteria for diagnostic and systematization of the fossil objects. The products of bacterial metabolic activity expressed by the lithology and geochemistry of rocks have special significance, and the study of carbon isotopes and other biomarkers has the highest importance. The main applications of traditional paleontology and bacterial paleontology differ strikingly. Bacterial paleontology is very important for sedimentology, and consequently for the study of the genesis of sedimentary mineral resources, including oil and gas. Bacterial paleontology also has importance for paleogeography in the study of epicontinental basins. The greatest significance of bacterial paleontological data is plain to see within the study of biosphere evolution, especially in the Precambrian and the Early Paleozoic. Finally, bacterial paleontology is one of the principle aspects for the study of astromaterials. For a more precise understanding of bacterial paleontology, geomicrobiology [24,25] needs to be addressed. The main task for any geomicrobiologist is to study the interrelation between bacteria or microorganisms on one side and rocks and minerals on the other. Certainly, the main biological objects of such works are recent organisms. Geomicrobiological studies are necessary not only for elucidation of the influence of recent microorganisms on the geological environment but also for the interpretation of fossil objects. Geomicrobiological studies have revealed that: • • •

Microorganisms actively affect all minerals without exception, forming biofilms on their surfaces, which, in turn, are essential features of the weathering process in a broad sense. Microorganisms can accumulate various metals. Microorganisms assist the formation of a variety of minerals that compose many sedimentary rocks, (including dolomite, layer silicates, and obviously calcium carbonate and phosphates).

Bacterial paleontology and geomicrobiology overlap in some areas; some geomicrobiological investigations are bacterial-paleontological and vice versa. These relationships are quite natural between closely related sciences. The recent electron-microscopy studies of rocks varying in chemical composition and age prove that fossilized microorganisms can be found in almost all sedimentary rock. The ancient phosphorites have become the classic objects for such studies. It is this study that has revealed the excellent state of preservation of diverse cyanobacteria and other microorganisms [14,17] (Fig. 1a and 1b). Parallel investigations treated rocks aged from the Archean to Quaternary, and microorganisms of uncertain nature were found in the Archean [5,28–30]. However, some strongly negative valuations [31] that repudiate some of the

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Figure 1. (a) Fragments of cyano-bacterial mat from Phosphorites (Khubsugul, Mongolia, Tommotian atage, Lower Cambrian). See differences in preservation (1. cyanobacterial tubes and 2. holes of tubes of cyanobacteria in purpule bacteries). (b) Cyanobacterial mat and purpul bacteria in phosphorits (Khubsugul, Mongolia, Tommotian stage, Lower Cambrian).

finds have been proffered. But, it seems, that the critics of the Shopff’s work may not have done it in a completely correct manner. The microorganisms from the Lower Proterozoic were found in the rocks of various types. The most interesting finds were made in jaspilites (BIF) (Fig. 2), shungites, cherty shales, and, certainly, in stromatolites. The presence of cyanobacteria in all of those rocks could almost be considered a proven fact. Going higher up the stratigraphic column, fossil bacteria have been found in the Vendian of the Russian Platform (Fig. 3(a)), the Lower Cambrian of Australia (Fig. 3(b)), Middle and Late Cambrian of the Siberian Platform (Fig. 3 (c) and (d)) [12], Ordovician Dyctionema Shales of the northwest Russian Platform, Domanik-like rock of the Ural region, and in thin clay layers in the Carboniferous of the Moscow Syneclise. Unique and somewhat unexpected results were obtained by the bacterialpaleontological study of graphite from the Botogol Deposit of East Sayan (South Siberia).

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Figure 2. Coccoids bacteria in BIF (Kursk Magnetic Anomaly, Lower Proterozoic).

Figure 3. (a) Cyanobacterial mat in Vendian of East European Platform, (b) cyanobacteria in Lower Cambrian (South Australia), and (c) and (d) cyanobacterial mats with filaments and coccoids (Lower Cambrian, Synyaya formation, Siberian platform).

For a long time, graphite of this deposit was considered to be magmatogenic, since the graphite bodies are hosted by nepheline-syenite. At first, tubular structures similar in shape and size to cyanobacteria were found in the graphite [19]. But the micron-sized tubes of very simply morphology did not convince the specialists on nepheline-syenites.

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Figure 4. (a) Fungi-bacterial assosiation in graphites of Botogol deposites (Devonian, E. Sayan, Siberia), (b)– (d) fragments of oribatid mites with trichobotrias in fungi-bacterial assosiation (Devonian graphites, Siberia), (e)–(f) trichobotria of mites (Holocen, Siberia) [32].

The study of this graphite continued [16], and in a short time, numerous fungal-like remains and fragments of loricate ticks with perfectly preserved trachybotria were found (Fig. 4). The finding of well-preserved ticks strongly supported the bacterial-paleonto-

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logical results and closed the discussion on the graphite origin. It is now obvious that these graphites were formed as the result of a conversion of highly carbonic sedimentary carbonate rocks. The deposits of sedimentary mineral resources give another perfect example of the tremendous role of bacterial in geological history. Besides the above mentioned phosphorites, jaspilites (BIF), graphites, and rare metal ores, the following rocks are noteworthy: iron ores, manganese ores (including oceanic manganese concretions), bauxites, sulfides, gold, etc. [13,33–36]. As already noted concerning Andrusov’s lectures, the bacterial role in the accumulation of iron (Fe), sulfur, silicon, phosphorous, and manganese (Mn) was undoubtful. Later it was realized that there are few elements in Mendeleev’s Periodical System (except for artificial elements and inert gases) that are not connected in some way with bacterial activity. The most striking example of the latest studies is the Tomtor rare metal deposit (Siberian Platform) [37]. Here cyanobacteria act as a specific filter, increasing the concentration of elements to tremendous levels: e.g., niobium content is 12 percent. It is clear today, that only a few species of bacteria are element-specific, and they extract a wide spectrum of elements from water. Two decades ago only ~20 minerals were known that were originated by the microbial activity [38]. The number of such minerals has grown significantly and now exceeds 100. Quartz, cristobalite, pyrolusite, silicates (including layered silicates), and feldspars are of special interest [13,22,25,39]. The biomineralization process in modern hot springs and in some terrestrial water basins convincingly demonstrate a rapid (minutes to hours) mineral formation with the participation of bacteria. Clear examples of authigenic bacterial mineralization were shown by Tazaki et al. [22]. Quartz, crystobalite, barite, feldspar, sulfur, buserite, ferrohydrite, hematite, pyrite, jarosite, smectite, kaolinite, calcite, and other minerals were discovered in differing environments of hot springs, lakes, mines, and waterfalls. In contrast to prior fragmentary data on these minerals, the Japanese discoveries are very impressive, and are described in their book [22]. Consider the example derived from the Hiraya hot spring. The spring was cased, and three groups of minerals were formed in a box and a tray where three bacterial communities (white, brown, and green mats) grew (Fig. 5 (a)). Changes in temperature, pH, and Eh values were measured (Fig. 5b). In the box with sausage-shaped bacteria (the white mat) located immediately at the hot spring, sulfur minerals of rhomboidal and amorphous form and fewer clay minerals, 7 Å, were formed. It has long been known that rhombic sulfur is generated with the participation of microorganisms. Two different mats occurred in the chute. The brown mat of filamentous bacteria and bacilli was in the axial part, where quartz, 3.3 Å; feldspar, 2.8 Å; cristobalite, 4.0 Å; and clay minerals, 7.0 Å, were formed. The green mat of filamentous bacteria functioned at the peripheral parts, where calcite, 3.0 Å; quartz; and clay minerals appeared. Thus in this case, it can be confidently stated that the bacteria participated in authigenic formation of the minerals listed—with some values, e.g.: those of pH, being registered. It should be stressed that diffractograms of mineral structure most frequently show a distinct hallo reflecting the amorphous phase of these minerals. Tazaki and his colleagues unambiguously noted the amorphous phase of the minerals. This makes the successive stages of mineral formation more clear. Among the many results that are now routinely published [24,25], those obtained by Gorbushina et al. [11] are most impressive. The researchers revealed that forsterite was formed with the participation of microorganisms, such as cyanobacteria, actinomycetes, and lichens.A very high rate (minutes to hours) of mineral formation was confirmed by numerous laboratory tests [13,20]. This can explain the excellent state of preservation of fossil

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Figure 5. (a) Illustration and (b) graphic representation of the distribution of different types of mats and minerals in Hiraya Hot Spring, Japan [22].

bacteria. In addition, the high rate of fossilization brought to attention a problem of dating the fossilization events; they could repeat over and over again in geological history. As already mentioned, the analysis of the x-ray structural data of the mineral phase of bacteria or inside bacterial mats revealed the presence of an amorphous mineral stage in

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Figure 6. Coccoidal bacteria (a) in clay and (b) with biofilm in clay (Carboniferous, Moscow basin).

most cases, except for carbonates. The amorphous stage is typical for minerals of the quartz group, Fe and Mn oxides, layered silicates, feldspars, etc. The amorphous stage is almost absent or unrecognizable by the x-ray structural method in calcite and aragonite. Probably, the preservation of fossilized bacteria is better when the amorphous stage is longer and more abundant. The worst preservation corresponds with carbonates since the

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Figure 7a. Lower Cambrian paleogeography of the Siberian platform. The index denotes (1) evaporite basins, (2) biogerms, (3) deep water basins, and (4) the boundary of the Siberian Platform) (after V. Savitsky and V. Astashkin).

cellular shells and membranes are destroyed by the rapid crystallization that occurs with a short amorphous stage. Carbonate micrites are usually believed to be products of microbial activity. Currently, the most interesting examples of bacterial formation of minerals are obviously referred to those minerals that are widely known as composing of sedimentary rocks, e.g.: clay minerals, feldspars, etc. Laboratory experiments and recent natural examples are already known [22]. However, the verification by data from the geological past is forthcoming. The first step in proving the idea concerning the authigenic formation of thin clay layers was the investigation by P.B. Kabanov, a specialist in the lithology and stratigraphy of Carboniferous deposits of the Moscow region. Kabanov used scanning electron microscopy to study the samples of thin layers from the Peski section (Fig. 6). The first illustration shows rounded bodies immersed within the unstructured matrix. It is noteworthy that all bodies are 2–5 µm in size and have a rounded shape. If it were terrigenous debris, the shapes would be obligatorily angular at such sizes. Therefore it must be supposed that they are coccoid bacteria. The second case is even more convincing. It was found that the rock is composed of spherical or granular bodies of 3–5 μm in size that are connected by thin threads. This situation is principally similar with the structure of the biofilms. Further study of the clayish rocks will present new evidence favoring the authigenic origin of most of them, especially the thin layers with inconstant spreading. The main problem is how to recognize and calculate ratios between terrigenous (probably more abundant) and authigenic-bacterial compounds of clay.

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Figure 7b. Lower Cambrian (Botomian) paleogeography of the Siberian platform [15].

In connection with the studies of clays, the problems of high-carbon rocks, including so-called black shale, become very important. The above-mentioned works on the Cambrian bituminous rocks of Siberia suggest that the earlier interpretation of such rocks being deep-water formations is dubious. The presence of benthic cyanobacterial remains in the Sinyaya Formation [15,40] forces the reinterpretation of the paleogeography of the Sinsk paleobasin. Instead of a rather deepwater basin opened towards the ocean, a shallow-water, partly closed sea with bottom anoxia (probably within the sediment) (Figs 7a and 7b) can be concluded. In addition to the biological evidences, the geological data also support this reconstruction. First, the boundary between the transitional zone and eastern part of the basin is clearly traceable within the middle reaches section of the Lena River. One has no chance to suggest a 400-m depth for the basin without ignorance of the structural geology and stratigraphy. Second, the sections of the Kolyma Masiff (although fragmentary ones) correspond to the transitional zone of the Siberian Platform in faunal and thickness characteristics. All of those facts induce a description of the general features of the ancient epicontinental basin. This type of the basin is absent from the recent environment. These basins covered a significant part of modern continents, mostly shallow water, and probably with intensive hydrodynamics that formed numerous short-lived and migrant islands. Owing to shallow water conditions and the fact that an entire water column was placed within the photic zone, the water masses were rich in bacteria. A study of paleogeographic reconstructions (Fig. 8) shows that such gigantic pools were typical for the Proterozoic and Paleozoic. They had nothing in common with the recent seas and oceans, so the character of sedimentation was different and, to a significant extent, was determined by bacterial (especially by cyanobacterial) activity.

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Figure 8. Distribution of epicontinental basins (black) in (a) Early Cambrian, (b) Early Ordovician, and (c) late Devonian.

All these data make a serious basis for the study of the biomorphic structures in meteorites. It was bacterial paleontology that gave a possibility to reconsider previous data and get new data on carbonaceous chondrites. A review of these data is present in several recent publications [13,41–43]. It is of special importance that all these works deal with objects of micrometric but not nannometric

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Figure 9. Principle events in the evolution of the Precambrian biosphere (after Rozanov, 1992, supplemented).

size. In addition, the problem of the recognition of contamination commonly present in meteorites was also discussed. Bacterial paleontology is a rather young branch of paleontological studies, but the first steps were made long ago. However, during recent years special bacterial-paleontological investigations have made it possible to formulate a series of six statements that significantly changed our conceptions in different areas of knowledge.

Conclusions 1. It has become clear that bacteria and microbes in general could be perfectly preserved as fossils since the period of their fossilization is minutes or hours. 2. It has been realized that the major part of the sedimentary rocks formed in the photic zone of epicontinental basins of the past originated under the influence of microorganisms and, in many cases, with a conclusive role of cyanobacterial communities. 3. Corresponding to the previous statement, sedimentary mineral resources, ores, and nonmetallics usually originate with significant assistance from microorganisms. 4. It has been realized that after special studies, the number of minerals formed with the participation of microorganisms has increased and is already >100. Some of these minerals are cristobalite, quartz, feldspar, layered silicates, oxides of Fe, and Mn. 5. It is clear that bacterial-paleontological data accompanied by data on the first origin of eukaryotes, metazoa, etc. significantly enrich the knowledge of evolution of the biosphere (Fig. 9), and reveal the long period of a transitional biosphere prior to the appearance of typical eukaryotic biosphere of modern type.

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6. It is understood that the bacterial-paleontological data on carbonaceous chondrites make a foundation for the possibility of the presence of extraterrestrial bacterial life. References [1] {[24]} American Mineralogist 1998; 83 11–2, 2, 1387–607. [2] {[33]} Amosov RA, Vasin SL, Kolesnikova EB. The role of the biological factors in accumulation of gold in the sedimentss. Ecosystem restructures and the evolution of biosphere, Moscow, PIN RAN 1995; 2: 147–53. [3] {[40]} Astafieva MM. Biomorphic microstructures in the Sinsk formation (Lower Cambrian of the Siberian platform), Proc. SPIE in press. [4] {[25]} Banfield JE, Nealson KH, editors, Geomicribiology: interactions between microbes and minerals. Reviews in Mineralogy 1997; 35: 448. [5] {[2]} Barghoorn TS, Tyier SA. Microorganisms from the Guntflint cherts. Science1965; 147 (3658): 563–77. [6] {[31]} Brasier MD, Green OK, Jephcoat AP, Kleppe AK, Van Kranendonk MJ, Lindsay JE, Steele A, Grassineau NV. Questioning the evidence for Earth’s oldest fossils. Nature 2002; 416: 76–81. [7] {[34]} Devouagard B, Posfai M, Xin Hua, Bazylinski DA, Frankel RB, Busek PR. Magnetite from magnetotactic bacteria: size distributions and twinning. American Mineralogist 1998; 83: 1387–98. [8] {[35]} Fortin D, Ferris FG, Scott SD. Formation of Fe-silicates and Fe-oxides on bacterial surfaces in samples collected near hydrothermal vents on the Southern Explorer Ridge in the northeast Pacific Ocean. American Mineralogist 1998; 83, 11–12, 2, 1399–408. [9] {[39]} Geptner AR, Petrova VV, Sokolova AL, Gorkova NV. Biochemical formation of layered silicates under hydrothermal changing of basalts, Iseland. Litologia i poleznye iskopaemye 1997; 2: 249–59. [10] {[20]} Gerasimenko LM, Goncharova IV, Zhegallo EA, Zavarzin GA, Zajtseva LV, Orleanskiy VK, Rozanov AYu, Tichomirova NS, Ushatinskaya GT. The process of mineralization (phosphatization) of filamental cyanobacteria. Litologia i poleznye iskopaemye 1996; 2: 208–14. [11] {[41]} Gerasimenko LM, Hoover RB, Rozanov AYu., Zhegallo EA, Zhmur SI. Bacterial Paleontology and Studies of Carbonaceous Chondrites. Paleontol. J. 1999; 33 (4): 439–59 (translated from Paleontol. Zhurnal 1999; 4: 109–25). [12] {[26]} Gerasimenko LM, Zavarzin GA. The relict cyanobacterial communities. In: The problems of preanthropogenic evolution of biosphere. Moscow: Nauka; 1993. 222–54 p. [13] {[21]} Gerasimenko LM, Goncharova IV, Zavarzin GA, Pochtareva IV, Rozanov AYu, Ushatinskaya GT. The Dinamic of release and absorbtion of phosphorus by cyanobacteria. In: Ecosystem changing and evolution of biosphere. Moscow: Nedra; 1994. 348–458 p. [14] {[11]} Gorbushina A, Boettcher M, Brumsack H-J, Krumbein WE, Vendrell-Saz M. Biogenic forsterite and opal as a product of biodeterioration and lichen stromatolite formation in table mountain systems (tepuis) of Venezuela. Geomicrobiol. J. 2001; 18: 117–32. [15] {[42]} Hoover RB, Rozanov AYu. Chemical biomarkers and microfossils in carbonaceous meteorites. Proc. SPIE 2002; 4495: 1–18. [16] {[3]} Kholl AH. Exeptional preservation of photosyntetic organisms in silicified carbonates and peats. Phil. Trans. R. Soc. London 1985; B311: 11–22. [17] Kirschvink JL, Jones DS, MacFadden BJ, editors. Magnetite biomineralization and magnetoreception in organisms. New York, London: Plenum; 1985. 2 p. [18] {[32]} Krivolutsky DA, Druk, Eitminaviciute IS, Laskova LM, Karppinen E. Fossil oribatid mites. Vilnius: Mokslas Publishers; 1990. 110 p. [19] {[38]} Lowenstam HA, Weiner S. On biomineralization. Oxford: Oxford Univ. Press; 1989. 324 p. [20] {[12]} Rozanov AYu. Fossil bacteria and new view on the processes of sedimentation. Soros Educational J. 1999; 10: 63–8. [21] {[13]} Rozanov AYu, editor. Bacterial paleontology. Moscow: PIN RAN; 2002. 188 p. [22] {[14]} Rozanov AYu, Zhegallo EA. On the problem of genesis of ancient phosphorites of Asia. Litologia i poleznye iskopaemye 1989; 3: 67–82. [23] {[15]} Rozanov AYu, Zavarzin GA. Bacterial paleontology. Vestnic RAN 1997; 67 (3): 241–5. [24] Rozanov AYu, Barskov IS. Diversity and phylum distribution of biominerals. In: Marfunin AS, editor. Advanced mineralogy v.3. Mineral matter in space, mantle, ocean floor, biosphere, environmental management and jewelry. Germany; 1998. 247–55 p. [25] Rozanov AYu, Barskov IS. Magnetite biomineralization, magnetofossils, and magnetoreception in organisms. In: Marfunin AS, editor. Advanced mineralogy v.3. Mineral matter in space, mantle, ocean floor, biosphere, environmental management and jewelry. Germany; 1998. 255–7 p.

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[26] {[16]} Rozanov AYu, Zhegallo EA, Hoover R. Microbiota of the botogol graphites. Proc. SPIE 1999; 3755: 38–46. [27] {[9]} Schopf JW, editor. Earth’s earliest biosphere: its origin and evolution. Princeton Univ. Press 1983, 544 p. [28] {[4]} Schopf JW. Microfossils of the Early Archean Apex Chert: new evidence of the antiquity of life. Science 1993; 260: 640–6. [29] {[5]} Schopf JW, Kudryavtsev AB, Agresti DG, Wdowlak ThJ, Czaja AD. Laser-Raman imagery of Earth's earliest fossils. Nature 2002; 416: 73–6. [30] {[6]} Schopf JW, Klein C, editors. The Proterozoic biosphaere: a multydisciplinary study. Cambridge: Cambridge Univ. Press; 1992. 1348 p. [31] {[7]} Sergeev VN, Knoll AH, Grotzinger JR. Paleobiology of the Mezoproterozoic Billiakh Group, Anabar Uplift, Northeastern Siberia. Journal of Paleontology 1995; 69, Memoir 39: 37 p. [32] {[8]} Sergeev VN. Silicificated microfossils of Precambrian and Cambrian of the Urals and middle Asia. Moscow: Nauka; 1992. 134 p. [33] {[10]} Sergeev VN, Kholl AH, Zavarzin GA. The first three billion years of life: from procariots to eucariots. Priroda 1996; 6: 54–67. [34] {[36]} Skinner HC, Fitzpatrick RW, editors. Biomineralization processes, iron, manganese. Cremlingen, Germany: Catena Verlag, Catena Suppl.; 21. [35] {[22]} Tazaki K, Aoki A, Asada R, etc. A new world in the science ofbiomineralization—enviromental biomineralization in microbial mats in Japan. Science Reports of Kanazawa Univ. 1997; 42 (1–2): 64. [36] Visscher PT, Reid RP, Bebout BM, Hoeft SE, Macintyre IG, Thompson Jr. JA. Formation of lithified micritic laminae in modern marine stromatolites (Bahamas): the role of sulfur cycling. American Mineralogist; 83, 11–12, 2, American Mineralogist 1998; 83, 11–2, 2, 1482–93. [37] {[1]} Vologdin AG. Geological activity of microorganisms. Izvestiya AN USSR 1947; Ser. Geol. 3: 19– 36. [38] {[28]} Walsh MM. Microfossils and possible microfossils from the Early Archean Onver-wacht Group, Barbeton Mountain Land, South Africa. Precambrian Res. 1992; 54: 271–93. [39] Weslall F, Rince Y. Biofilms, microbial mats and microbe-particle interactions: electron microscope observations from diatomaceous sediments. Sedimentology 1994; 41: 147–62. [40] {[23]} Westall F, Boni L, Guerzoni ME. The experimental silicification of microorganisms. Paleontol. 1995; 38: 495–528. [41] {[29]} Westall F, Walsh MM. Early Archean fossil bacteria. In: Bacterial paleontology. Moscow: PIN RAN; 2002. 84–90 p. [42] Yates KK, Robbins LL. Production of carbonate sediments by a unicellular green algae. American Mineralogist 1998; 83, 11–2, 2, 1503–9. [43] {[27]} Zavarzin GA. Bacteria and the composition of biospere. Moscow: Nauka; 1984. 199 p. [44] Zhang Ch, Vali H, Romanek ChH, Phelps TJ, Liu ShV. Formation of single-domain magnetite by a thermophilic bacterium. American Mineralogist 1998; 83: 1409–18. [45] {[17]} Zhegallo E.A. et al. Atlas of microorganisms from ancient phosphorites of Khubsugul (Mongolia). Huntsville, Alabama: NASA; 2000, 167 p. [46] {[18]} Zhmur SI, Rozanov AYu, Zhegallo EA, Lobzova RV. Cyanobacterial benthic system—the producent of carbonaceous material of shungites of the Lower Protherozoic of Karelia. Litologia i poleznye iskopaemye 1993; 2: 122–4. [47] {[43]} Zhmur SI, Rozanov AYu, Gorlenko VM. Lithified remaines of microorganisms in carbonaceous chondrites. Geochimia 1993; 1: 66–8. [48] {[37]} Zhmur SI, Rozanov AYu, Kravchenko SM, Zhegallo EA. About genesis of rich rare-earth ores of Tomtor (the north of the Siberian platform. Reports RAN 1994; Ser. geol., 336 (3): 372–5. [49] Zhmur SI, Rozanov AYu, Sokolov BS, Bazhenova OK, Gorlenko VM. Bacterial mats as a resource of the maternal mater of oil. Moscow: DAN RAN 1994; 6: 742–4. [50] {[19]} Zhmur SI, Rozanov AYu, Lobzova RV, Zhegallo EA. About resource of carbon of graphite ores of Botogol sienite massif (East Sayan). Moscow: DAN RAN 1996; Ser. Geol., 348 (3): 360–2. [51] {[30]} Zhmur SI, Duda VI, Skryabin GK, Roizeman FM. Microfossils in Early Archean graphites of Aldan Shield and some aspects of panspermia [4495–04]. Proc. SPIE 2002; 4495: 19–26.

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Perspectives in Astrobiology R.B. Hoover et al. (Eds.) IOS Press, 2005 © 2005 IOS Press. All rights reserved.

Paleobiological and Biogeochemical Vestiges of Early Terrestrial Biota: Baseline for Evaluation of Extraterrestrial Evidence Manfred SCHIDLOWSKI Max-Planck-Institut für Chemie (Otto-Hahn-Institut), Abt. Biogeochemie, Postfach 3060, D–55020 Mainz, Germany Abstract. Based on the currently known paleontological and biogeochemical record of life in the oldest terrestrial sediments and moderate extrapolations thereof, it may be stated with fair confidence that microbial (prokaryotic and archaeoprokaryotic) ecosystems had been prolific on early Earth from at least 3.8 Ga ago. While the information encoded in the oldest record (>3.5 Ga) is commonly impaired by a metamorphic overprint, the evidence for the existence of life at times <3.5 Ga seems so firmly established as to be virtually unassailable. This holds for both the morphological (cellular) record and the biogeochemical data. Specifically, the 13C/12C signature of fossil organic carbon conveys a remarkably consistent signal of biologically mediated (enzymatic) carbon isotope fractionations over ~4 Ga of recorded geological history, suggesting an extreme degree of evolutionary conservatism in the biochemistry of (photo) autotrophic carbon fixation. Postulating a universality of biological principles in analogy to the proven universality of the laws of physics and chemistry, it may be reasonably expected that the principal properties of extraterrestrial life are similar to those that characterize Earth-bound biology. Hence, the record of life preserved in Earth‘s oldest sediments should provide a sound baseline for the interpretation of extraterrestrial analogues. Inter alia, enzymatic reactions in exobiological systems ought to be beset with isotopic fractionations resembling those in earthly biochemistry, with 13C/12C values eventually retrieved from Martian rocks likely to constrain current conjectures on the existence of former life on Mars.

Introduction Since Kepler and Newton established the fundamentals of celestial mechanics with the identification of gravity as the underlying force, it became increasingly clear that the principles of physics that rule Earth are also valid for the solar system at large. About 2 centuries later, Bunsen opened up a broad window to the chemistry of the Sun and the stars by means of spectral analysis, and reached the conclusion that the very chemical elements known on Earth also abound on other celestial bodies. By now, it is part of confirmed knowledge that the laws of physics and chemistry are universal, holding dominion over the Cosmos as it is known today. Considering the proven universality of the laws of physics and chemistry, it seems justified to also postulate a universality of the basic principles on which life processes are

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based. There is a general consensus today that life had emerged at a certain stage of either cosmic or planetary evolution as an intrinsically new property of matter [1–4]. In general, life processes are non-equilibrium processes, remote from the thermodynamic equilibria that prevail in their environment. They are characterized by what is called metabolism, which is the absorption of matter and energy to build up local domains of lower (negative) entropy—in fact, life can be aptly defined in terms of its entropy-deferring properties. Consequently, such metabolic centers developed the tendency to fence themselves off from the outside world by the design of suitable membrane systems, which finally resulted in the establishment of the cell as the smallest morphological and functional entity of life. Accordingly, life expresses itself morphologically in the form of discrete structures or compartments distinct from the unorganized or amorphous state of its inorganic environment. Apart from their morphological distinctions and their persistence as dynamic states removed from thermodynamic equilibrium to markedly lower entropy levels, living systems are further characterized by their preferential reliance on a limited set of chemical elements (notably, carbon, oxygen, hydrogen, nitrogen, sulfur, and phosphorus), and their capability of proliferation by means of identical reproduction that is based on the chemistry of nucleic acids (notably, five distinct nucleotide bases and eight nucleotides). Moreover, the chemistry of life in general or biochemistry is contingent on the presence of water to such an extent that the lack of water can be equaled with the non-existence of life. Conversely, the presence of liquid water may be taken as a surrogate indicator or proxy of life as the axiom ubi aqua, ibi vita (where water is, there is life) is almost self-evident to the chemist. In fact, water is a very peculiar solvent. Theoretically, the compound H2O ought to exist in gaseous form at normal temperature and pressure. Its actual existence as a liquid under these conditions is due to the fact that the H2O molecules are capable of establishing hydrogen bonds among each other, with the resulting polymeric network being so tightly interwoven as to raise the boiling point from a theoretical 40 ˚C to the actual level of 100 ˚C. Also, water may establish hydrogen bonds with a host of organic substances, which are then water-soluble. In contrast, other classes of organic substances, such as hydrocarbons, are unable to form such hydrogen bonds, being, consequently, water insoluble. Hence, there exists a marked dualism in the behavior of organic substances with regard to water that is reflected by the contrasting terms hydrophilic and hydrophobic. This dualism has been shown to crucially promote the three-dimensional buildup of many biopolymers. Further, the high dielectric constant and the dipole character of the single H2O molecule substantially add to the chemical potential of water as a principal agent in biochemical reactions. In concert, all of these properties assign a key role to water in any form of biochemistry [5]. It should be stated explicitly that only Earth-based life is known, and perhaps basically understood, but it seems reasonable conjecture that life-like processes in other cosmic settings are grounded on the same principles. Hence, the basic properties of life as we know it from Earth should provide a powerful guideline in the search for manifestations of life-like phenomena on a cosmic scale, whether extant or fossil. It follows from the previous argument that there are two principal routes to track down the possible presence of life in extraterrestrial settings inclusive of its fossil manifestations (such as expected, for instance, in sediments formed during an early water-rich period of Mars): 1. One should look for morphological evidence indicative of life and organisms in the widest sense. As long as one deals with the microbial world, a prime target would be the morphology of the bacterial cell. There is ample evidence that the bacterial cell readily lends itself to fossilization under a set of favorable circumstances. 2. A second line of investigation should focus on the search for remnants of the metabolism of ancient organisms, capitalizing on the fact that life processes rely on a

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very small selection of chemical elements of which carbon is the most prominent. Hence, conspicuous accumulations of reduced carbon, and, notably, their isotopic (13C/12C) compositions might constitute potential evidence of former life if encountered in appropriate sedimentary settings on other celestial bodies. This also holds for single, discrete carbon compounds, which have braved the hardships of the fossilization process and preserved their molecular identity in the face of increasing metamorphic temperatures and pressures (called chemofossils or chemical biomarkers). Such biomarker compounds are exceptionally stable molecular structures, mostly organic pigments like porphyrins or single, discrete hydrocarbon chains of known biological origin.

1. Statement of Problem For any forthcoming fossil hunt on Mars, we would be well advised to make full use of the information stored in the micropaleontological and biogeochemical inventories of the oldest (Archean) terrestrial sediments, that is, those covering the time window of 3.3–3.8 Ga. These rocks are roughly coeval with the sedimentary formations deposited in the water-rich environment of juvenile Mars as documented by the water-carved surface morphology that is exposed on large parts of the outer face. If it is true that Earth and Mars had occupied roughly comparable starting positions in terms of environmental conditions and the endowment with matter from the parent solar nebula, then the surficial scenarios on both planets should have been very similar in their youthful states. With ample evidence available for a denser atmosphere and extensive aqueous activity during early Martian history, a convincing point can be made that the primitive Martian environment was not less conducive to the initiation of life processes and the subsequent establishment of prolific microbial ecosystems than the surface of juvenile Earth. Even if the evolutionary pathways of both planets had diverged during their later histories so that life became extinct on Mars due to the establishment of surface conditions inhospitable to protein chemistry, one could still entertain the notion that the planet had originally started off with a veneer of microbial (archaeoprokaryotic and prokaryotic) life comparable to that documented for Archean Earth. Hence, a prime objective for exobiological work on Mars should be a targeted search for extinct life, and the oldest Martian sediments should provide an appropriate test ground for such efforts. The crucial difficulty in any search for fossil manifestations of life on Mars certainly does not rest with the cognitive approach to the presumptive evidence (either morphological or biogeochemical), but rather with the serendipity of the encounter of suitable sampling material among the vast stretches of potential host rocks exposed on the planet’s surface. However, unlike the selection of the sites for the Viking life detection program that largely resembled a shot in the dark, the chances for the detection of ancient life are proportionately enhanced by the fact that two-thirds of the Martian surface appear to be covered by rocks older than 3.8 Ga [6]. Among these surface exposures are apparently well-bedded sediments (notably, in the Tharsis region and the associated Valles Marineris canyon system) that have been interpreted as lake deposits and are believed to include thick carbonate sequences [7]. It may reasonably be assumed that any morphological and chemical vestiges of fossil life would lend themselves to as ready a detection in these early Martian formations as they do in terrestrial (inclusive of Archean) sediments by either robotic sensing or, better still, direct investigation following a sample return mission. Any systematic search for relics of former life, specifically in Martian sediments, that is calibrated on fossil evidence from the oldest terrestrial record should focus on two categories of paleobiological documents. The first is structural evidence pertaining to the mor-

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Figure 1. Principal categories of paleobiological evidence documented over 3.8 Ga of geological history. The Hadean Eon at the beginning of the time scale covers the window between the formation of planet, 4.56 Ga, and the onset of the sedimentary record; the Archean and Proterozoic Eons are conventionally summarized as Precambrian. Note start of sedimentary record at ~3.8 Ga with the segment t>3.5 Ga (broken line) bearing a metamorphic overprint that affects the preservation state of microfossils (2) leads to a graphitization of sedimentary organic carbon (3) and is bound to reset the 13C/12C signal of (photo) autotrophic carbon fixation commonly retained in nonmetamorphosed sedimentary organic carbon or kerogen (4). Fossil relics of laminated microbial ecosystems or stromatolites (1) have not yet been discovered in rocks older than 3.5 Ga; the extension to 3.8 Ga of the microfossil record (2) is conditional on the acceptance of the biogenicity of the principal cell-like morphotype, Isuasphaera isua, from the Isua suite.

phology of the bacterial cell in the widest sense. Apart from the morphology of the individual cell, the morphological manifestations of fossil cell aggregates or microbial communities are decidedly relevant. As a rule, microbes are not solitary organisms, they are extremely social with a strong tendency to stick together and form extended microbial mats, such as those typically occurring at the sediment-water interface in certain aquatic environments. The second category is represented by chemical relics of former life. These are primarily carbonaceous (in part graphitic or pre-graphitized) residues of ancient organisms with their intrinsic 13C/12C ratios, and single recalcitrant carbon compounds of attested biological pedigree that have survived the wholesale reconstitution of primary organic matter in the sediment. In the following, a review will be given of the principal manifestations of these two categories of fossil evidence in the oldest terrestrial sediments. Armed with this background information, one should be well prepared for a judicious assessment of possible vestiges of fossil life from extraterrestrial settings.

2. Paleobiological Evidence in the Terrestrial Rock Record Generally, any biosphere that spans the surface of a planet is apt to leave discrete vestiges in the surrounding inorganic habitat. Relying on the terrestrial rock record, it may be taken for granted that living organisms leave a whole set of morphological and chemical traces in sedimentary rocks. Though, in part, highly selective, this record may survive over billions of years before being ultimately annealed as a result of a metamorphic or an anatectic reconstitution of the host rock. This is not only true for higher (multicellular) life (Metazoa and Metaphyta) characterized by a formidable preservation potential but also, albeit with restrictions, for microorganisms [8], which had dominated Earth’s biosphere over the first 3 Ga of recorded geological history. Figure 1 gives an overview of the principal categories of paleobiological evidence over Earth’s history that are relevant for this argument.

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Figure 2. Filamentous biomorphs of putatively cyanobacterial affinity from the Archean Warrawoona microflora of Western Australia (3.46-Ga-old Apex chert). These currently disputed microstructures have been described by Schopf as (a) and (b) Primaevifilum amoenum, (c–f) Archaeoscillatoriopsis disciformis, and (g) Primaevifilum delicatulum [13].

2.1. Morphological Evidence of Early Terrestrial Life: The Paleontological Record Dealing primarily with the microbial world at the very beginning of geological history, the following discourse will restrict itself to the micropaleontological (preferentially cellular) record of ancient life. The record of cellular microfossils goes, surely, back to >3 Ga ago, with the beginnings blurred by either 3.5 or 3.8 Ga, depending on the prevalent prejudices of the single working group or school of thought, respectively. While a wealth of authentic microbial communities has been reported from Early and Middle Precambrian (Proterozoic) formations, the unequivocal identification of cellular microfossils becomes notoriously difficult with the increasing age of the host rock. In Early Precambrian (Archean) sediments, both the progressive diagenic alteration and the metamorphic reconstitution of the enclosing mineral matrix tend to blur the primary morphologies of delicate organic microstructures. This results in a large-scale loss of contours and other critical morphological detail. The extremes of such alteration series are represented by so-called “dubiofossils” of variable and sometimes questionable confidence levels. To ascertain the biogenicity of possible cellular morphotypes in Archean rocks, a hierarchical set of selection criteria has been proposed, postulating that genuine microfossils (1) be authentic constituents of the rock as testified by their exposure in petrographic thin sections, (2) occur in vast multiples, (3) be associated with residual carbonaceous matter, (4) equal or exceed the minimum size of viable cells and display a central cavity plus structural detail in excess of that resulting from inorganic processes. Moreover, it has been proposed that, as a matter of principle, putative evidence from metamorphosed sediments should not be considered. In spite of the blatant impoverishment of the Archean record, there are, however, single reports of well-preserved microfossils that, for the most part, comply with the above criteria. Most prominent among these assemblages are chert-embedded microfloras from the Warrawoona Group of Western Australia, which closely approach the 3.5 Ga age mark (Fig. 2). After an initial controversy about the authenticity of these fossil communities on

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Figure 3a. Comparison of Huroniospora sp. from the ~2.0-Ga-old Gunflint iron formation, Ontario (1)–(3) with Isuasphaera sp. from the ~3.8-Ga-old metasediments of the Isua Supracrustal Belt of Greenland (4)–(6)—the optically distinctive marginal rim displayed by some of these biomorphs can be explained as a relic of the original cell wall—and (b) Laser Raman spectra obtained from Huroniospora species (sp.) as an isolated particle (1) and in thin sections (2) compared to those from Isuasphaera sp. (3) and (4) obtained under the same conditions. The close resemblance of the spectra suggests similarities in the composition of the residual organic component of the two types of microstructures. The prominent peak, close to 1,610 cm –1, is indicative of aromatic double bonds among the carbon atoms of the molecular structure [25].

the grounds of imprecisely constrained petrographic background parameters for the host lithologies [9,10], Schopf and Packer [11], and, notably, Schopf [12] subsequently forwarded evidence prompting an acceptance of the observed morphotypes as bona fide microfossils. Conspicuous within the Warrawoona microbial community are both the coccoidal and filamentous (trichomic) micromorphologies that have been found to abound in the cyanobacterial precursor floras of Proterozoic formations. While the septate filaments were supposed to stand for fossil trichomes that could be attributed to either filamentous cyanobacteria or more primitive prokaryotes, such as flexibacteria, the coccoidal aggregates described by Schopf and Packer [11] have been claimed to strictly exclude other-thancyanobacterial affinities. Cellular microfossils of various confidence levels have also been reported from other Archean terrains, notably southern Africa [14–18]. Given the remarkable degree of diversification of these Archean microfloras, it must, of necessity, be inferred that the genetic lineages of the principal microbial species had emerged well before Warrawoona times. It may, therefore, reasonably be assumed that precursor floras had been extant prior to ~3.5 Ga, when the preserved rock record becomes scant and increasingly metamorphosed. In this context, the observation of cell-like carbonaceous structures in the 3.8-Ga-old metasediments from the Isua Belt of Greenland, has attracted considerable attention. Described as Isuasphaera isua [19], the biogenicity of this morphotype (Fig. 3) had been violently disputed, specifically, on the grounds of the improbability of the survival of delicate cell structures during the amphibolite-grade metamorphism of the host rock [20]. Meanwhile, however, there is ample evidence that fossils in general and microfossils in particular may—in variable degrees—withstand obliteration in rocks subjected to medium-

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grade metamorphism [22]. Therefore, one cannot a priori exclude microbial affinities for selected cell-like microstructures from the Isua metasediments, and notably, for Isuasphaera-type micromorphs that show a striking resemblance to a possible counterpart of recognized biogenicity in the younger (Proterozoic) record described as Huroniospora sp. In spite of the uncertainty surrounding a large number of morphotypes described from Isua and of occasional convergences with purely mineralogical features, there is a reasonable chance that the microstructure inventory as a whole includes at least some elements of a structurally degenerated microfossil-assemblage, such as might result from metamorphic impairment of a Warrawoona-type microflora. Anyhow, the existence, in Isua times, of microbial ecosystems would not only be consistent with, but also conditional for, the actually observed carbon content and carbon isotope geochemistry of the Isua suite. While the 3.8-Ga-old Isua morphologies have been under heavy debate since the early 1980s [20], severe criticism has recently also centered on the chert-hosted microbial community of the younger Warrawoona System, which had figured as the very paragon of an Archean microflora over the last decade [13]. Questioning the hospitability as a microbial habitat of the primary hydrothermal environment of the fossiliferous Apex cherts and dismissing the morphology of the septate filamentous structures as intricate mineralogical artifacts, Brasier et al. [23] have voiced doubts as to the very facticity of the purported Warrawoona microflora as a whole, inclusive of its inferred cyanobacterial connection. Moreover, Brasier and coworkers also deny the diagnostic relevance of laser Raman spectroscopy for determining the biogenicity of structured organic carbon remains for which this technique had been utilized to correlate the carbon chemistry with optically discernible microbial morphologies [24]. The strong degree of opinionating evident in this controversy certainly shows that this, as in the case of Isua, is an actively evolving science frontier, which still leaves room for opposing standpoints. Naturally, there is no doubt that a host of petrographic, microstructural, and microanalytical work remains to be executed to secure the cognitive underpinnings of current efforts to identify authentic microbial objects in ancient rocks, notably in those bearing a hydrothermal or metamorphic overprint. On the other hand, the balance of the presently known paleobiological evidence clearly argues for an early initiation of life process on this planet. Even if the Warrawoona microflora were discredited, which some schools of thought will violently deny, this would not necessarily affect the validity of the South African (Barberton) evidence, which also broadly covers the time window of 3.3–3.5 Ga ago and had been largely eclipsed over the last years by the well-documented and well-publicized Warrawoona micromorphs, whose fairly narrow time constraints (~3.465 Ga) made them slightly older than the other putative Archean microfloras. Hence, even with a disputed Warrawoona flora, there is no need for a fundamental revision of the basic concepts of early organic evolution on Earth as they had evolved over the last decades [25,26] except for a revision of the hitherto proposed timetable for the probable advent of cyanobacteria. A second category of paleontological evidence that gives testimony to the existence of microbial life during Earth’s earliest history is represented by organosedimentary structures of the stromatolic type. Stromatolites or microbialites [27] are stratiform microbial buildups that have preserved the matting behavior of bacterial and algal, primarily prokaryotic, microbenthos in the sediment. Microbial buildups of this type represent stacks of finely laminated lithified microbial communities that had originally thrived as organic films at the sediment-water interface, with younger mat generations successively superimposed on the older ones (Figs 4 and 5). The structures derive from the interaction of the primary biologically active microbial layer with the ambient sedimentary environment, and the fossilization of the laminae results from trapping, binding, or biologically mediated precipitation of selected mineral constituents.

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Figure 4. Scheme of principal morphologies of laminated microbial ecosystems, which colonize the sediment-water interface in selected aquatic environments. These structures subsequently lend themselves to lithification in the form of stromatolites (Fig. 5). The mat-forming microbenthos is mostly made up of cyanobacteria.

Figure 5. Typical stromatolite showing distinct lamination and parallel columns with digitate branching from the Paleoproterozoic of the Labrador Trough (Canada) (collected by D.M. Mossman)—about half natural size.

In terrestrial sediments, microbialites represent the most conspicuous (macroscopic) expression of fossil microbial life, with a record extending back to the Early Archean, ~3.5 Ga ago. This constitutes prima facie evidence that benthic prokaryotes were already widespread in suitable aquatic habitats of Archean Earth. Both the morphological inventory of the oldest stromatolites and the observed microfossil content of the ambient rock or coeval sequences allow a fairly elaborate reconstruction of Earth’s earliest microbial ecosystems, indicating that Archean stromatolite builders were not markedly different from their geologically younger counterparts (inclusive of contemporary species). It appears well established that the principal microbial mat builders were filamentous and unicellular pro-

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Figure 6. Formation of polycondensed heterogeneous geopolymers (kerogen) from primary biopolymers of dead organic matter. The pathway of kerogen formation comprises a catabolic branch furnishing breakdown products on the monomer level and an anabolic branch promoting the recombination of these fragments to give rise to a new generation of nonbiological carbon polymers (geopolymers) represented by kerogenous substances.

karyotes, capable of phototactic responses and probably of photoautotrophic carbon fixation [28]. The unbroken stromatolite record from Archean to present attests, furthermore, to an astounding degree of conservatism and uniformity in the physiological performance and communal organization of prokaryotic microbenthos over 3.5 Ga of geological history. In spite of recently voiced reservations elaborating on morphological convergences between biologically induced and purely inorganic (evaporite and microclastic) laminations [29], the balance of the currently available evidence suggests that the oldest stromatolites constitute a crucial if not dominant part of the early record of life [30]. 2.2. Chemical Evidence of Early Terrestrial Life: The Biogeochemical Record Apart from morphological or structured relics, organisms also leave a chemical record of their former existence. When they die, their organic substance degrades with a concomitant loss of order, with the carbon component almost completely remineralized to CO2. What escapes remineralization by burial in sediments are commonly between a few per mil to ~1% of the original carbon fraction, which are destined to end up as sedimentary organic matter or kerogen, respectively. Likewise, traces of single-refractory or die-hard molecular architectures (mostly pigments like porphyrins and single discrete hydrocarbon chains) may survive the fossilization process, attesting to the biogenicity of the precursor materials as so-called biomarker molecules. 2.2.1. Sedimentary Organic Matter (Kerogen) Actually, in dead organic matter, the complex network of biopolymers breaks down into its monomers, which in turn, may partially recombine during the diagenetic reconstitution of the organic debris within the sediment to give rise to a completely novel brand of inorganic carbon polymers (geopolymers), commonly summarized under the term kerogen (Fig. 6). Kerogen, as a thoroughly reconstituted modification of sedimentary organic matter [31], is a chemically inert, i.e.: acid insoluble, polycondensed aggregate of aliphatic and aromatic hydrocarbons that figure as end products of the diagenetic alteration of primary biogenic substances in the sediment. With about 1.2×1022 g of kerogenous (reduced) carbon stored in Earth’s sedimentary shell, kerogen is the most abundant form of organic matter on this planet. Representing the residuum of living matter, kerogenous materials and their graphitic derivatives constitute per se first-order proxies of past life processes. Moreover, kerogenous

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substances tend to preserve the carbon isotopic composition of their biological precursor materials, which are, throughout, characterized by a marked bias in favor of the light carbon isotope, 12C, relative to the heavy one, 13C. 2.2.2. Isotopic Geochemistry of Sedimentary Organic Carbon Generally, life processes are characterized by a change from a largely stochastic chemistry, where substances react with each other in a way that is governed by chance or probability, to a new kind of algorithmic chemistry, where reactions follow a set of predetermined and quasi-fixed repetitive patterns, with homochirality and self-replication figuring as the principal innovations [32]. As a consequence, organisms synthesize biogenic matter with a high degree of structural specificity and a limited distribution of structural types. The high degree of order typical of organic substances is manifest on both the intermolecular and intramolecular levels, being evident in the form of redundant molecular abundance patterns, sequencing, stereochemistry, and—last but not least—in a large variety of isotopic preferences. This is particularly true in the case of carbon. Constituting the key element of life, carbon principally consists of a mixture of two stable isotopes, one light, 12C, and one heavy, 13 C. (A third, short-lived radioactive nuclide, 14C, occurs only in trace amounts.) 12C, the isotopically light carbon variant accounts for about 98.9% of the total abundance, while the balance of 1.1% is made up by heavy variant, 13C. 2.2.2.1. Origin of Biological Carbon Isotope Fractionations Since the pioneering work by Nier et al. [33,34] it is known that the incorporation of inorganic carbon into living systems involves sizeable fractionations of the stable carbon isotopes that have made the bulk of biologically processed carbon isotopically lighter, 12C enriched, as compared to the carbon compounds of the inorganic feeder pool and the nonliving world. In fact, the largest carbon isotope effects have been shown to occur during biological assimilation of inorganic carbon in the various pathways of autotrophic, specifically photosynthetic, carbon fixation. This is primarily the incorporation of carbon dioxide (CO2) and bicarbonate ion (HCO −3 ) by plants and microorganisms that proceeds by a limited number of biochemical pathways and carbon-fixing reactions (Table 1). Meanwhile, a wealth of investigations [35–40] have confirmed that all common assimilatory pathways, specifically the photosynthetic ones, discriminate against 13C, mostly as a result of a kinetic isotope effect inherent in the first irreversible enzymatic CO2-fixing reaction. Since assimilatory pathways are largely enzyme-controlled and living systems as such constitute dynamic states undergoing rapid cycles of anabolism and catabolism, it is generally accepted that most biological isotope fractionations are due to kinetic rather than to equilibrium effects (for solitary dissent see Walker [41]). Quantitatively, the differences in these fractionation processes are expressed in terms of the conventional δ-notation that gives the per mil deviation in the 13C/12C ratio of a sample (sa) relative to that of a standard (st), i.e.:

δ 13 C = [

(13 C/ 12 C) sa – 1]× 1,000(‰, PDB). (13 C/ 12 C) st

(1)

The standard defining zero per mil on the δ-scale is Peedee belemnite (PDB) with C/13C=88.99. Positive values of δ 13C in a sample indicate an enrichment in 13C relative to this standard, while negative values stand for a depletion in 13C. Kinetic isotope fractionations reflect differences in either the reaction of translocation rates between the heavy and the light carbon isotopes and are primarily imposed on two steps in the primary metabolism of autotrophic organisms: (1) the diffusion of external CO2

12

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Table 1. Pathways of biological carbon fixation responsible for the conversion of CO 2 and CH4 into living biomass. Reactions (1)–(4) are carbon-fixing carboxylation reactions utilized in common autotrophic pathways in which reduction of CO2 primarily yields C3 compounds (with 3-carbon skeletons, such as phosphoglycerate and pyruvate), C4 compounds (oxaloacetate), and C2 compounds (acetate and acetyl coenzyme A). In methanotrophic pathways (5) and (6), carbon assimilation proper is preceded by oxidative transformation of CH4 to HCHO (formaldehyde). Adapted and updated from Schidlowski et al. [35].

to the assimilatory centers, and (2) the first irreversible enzymatic fixation of CO2 in the carboxyl (COOH) group of an organic (carboxyclic) acid (Fig. 7). On the other hand, thermodynamically controlled equilibrium fractionations determine the isotope exchange be−

tween CO2 and HCO 3 in bicarbonate-utilizing pathways, such as C4 and Crassulacean acid metabolism (CAM) photosynthesis [42] where bicarbonate ion serves as the active feeder species. Moreover, equilibrium fractionations have been proposed to also govern the intermolecular and intramolecular isotope exchange among different classes of biosynthesized metabolites, such as proteins, carbohydrates, and lipids. With the uptake and intracellular diffusion of external CO2 and the subsequent CO2fixing carboxylation reaction constituting the principal isotope-selecting steps in the assimilatory process, the essentials of biological carbon isotope fractionation may be summarized, with adequate approximation, by the two-step model shown in Fig. 7. In summary, the individual fractionations bring about a sizeable shift in the δ13C values of biosynthesized matter towards negative readings relative to CO2 of the external feeder pool. The largest single fractionation effect commonly derives from the isotope-discriminating properties of the carboxylating enzymes operative in the second step. The overall isotope shift can be ex-

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Figure 7. Principal isotope-discriminating steps in biological CO2-fixation (black: assimilatory reactions; stippled: dissimilatory and other reverse processes; k1–k4: corresponding rate constants). Carbon dioxide from the external (atmospheric) feeder pool [CO2(e)] enters the living tissue to become internal CO2(i) on its way to the photosynthetically active sites, and is subsequently transformed to R-COOH that stands for the product of the first CO2-fixing enzymatic carboxylation reaction. In sum, these processes lead to a preferential enrichment of light carbon (12C) in organic substances relative to the feeder substrate; the largest single effect is associated with the enzymatic carboxylation step.

pressed as the difference between the isotopic composition of the cells and that of the inorganic substrate, i.e.: Δ = δ 13 C cells – δ 13 C CO 2 [‰] .

(2)

The kinetic isotope effect imposed on the initial diffusion step (Fig. 7, specifically k1 and k2) discriminates only slightly against 13C, attaining as a maximum the value for CO2 diffusion in air (–4.4‰). Since the pure effect of gaseous diffusion is commonly modulated in the natural environment by dissolution, hydration and liquid transport of CO2, actually observed fractionations usually stay well below this maximum. With liquid diffusion considerably retarded as compared to the gaseous process, the concomitant isotope effects are commonly small, from –1.6 to –3.2‰, or may even approach unity with a few tenths of a per mil [38,39]. Such minor fractionations have been specifically observed in aquatic plants and microorganisms, whose carbon-fixing pathways are largely diffusion limited [40,43]. Fractionations in the subsequent enzymatic carboxylation step (Fig. 7, specifically k3) are, on the other hand, significantly larger but highly variable in detail. In the case of the quantitatively dominant ribulose-1.5-bisphosphate (RuBP) carboxylase reaction (Table 1), the magnitude of the isotope effect has been shown to mostly range between –20 and –40‰. This extended range obviously derives from the fact that fractionations in enzymatic reactions vary widely as a function of pH, metal cofactor, temperature, and a number of other variables [44]. Since the carboxylation product emerging from this reaction is a compound with a 3-carbon skeleton (phosphoglycerate) that immediately enters the reductive pentose phosphate or Calvin cycle, the corresponding pathway has been termed C3 or Calvin cycle photosynthesis. The Calvin cycle constitutes the principal contrivance for the biologically mediated reduction of CO2 to the carbohydrate level that channels most of the carbon transfer from the nonliving to the living world. Apart form eukaryotic algae and the bulk of photoautotrophic and chemoautotrophic bacteria, it is utilized by all green plants; those that rely on it exclusively are called C3 plants. A quantitatively less important carboxylation reaction that fixes CO2 as a 4-carbon compound (oxaloacetate) is catalyzed by the enzyme phosphoenolpyruvate (PEP) carboxylase (Table 1). This carboxylation figures as the initial carbon-fixing reaction in the C4 dicarboxylic acid or Hatch-Slack pathway and entails only a minor discrimination against 13C on the order of –2 to –3‰, relative to the bicarbonate ion that serves as the active feeder species in this particular case. Plants utilizing this pathway are termed C4 plants and are basically represented by tropical grasses, including two important agricultural crops, maize and sugar cane. As a whole, C4 species are markedly 13C enriched, i.e.: isotopically heavy, as compared to higher plants that rely on C3 photosynthesis (Fig. 8). The isotope effects brought about by some ferredoxin-linked carboxylation reactions of minor quantitative importance that rely on CO2 acceptors, such as succinyl coenzyme A and acetyl coenzyme A,

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Figure 8. Carbon isotope spreads of major groups of higher plants and microorganisms (stippled) as compared to respective spreads of the principal inorganic carbon species (CO 2, HCO −3 , CO 2− 3 ) in the environment (black). Triangles indicate approximate means. Note consistently negative δ13C ranges of biological materials implying an enrichment in light carbon, 12C, relative to the inorganic feeder species, mostly CO2.

are as yet poorly known, but fractionations observed with organisms that have these reactions integrated into their assimilatory pathways, such as the green photosynthetic bacteria or Chlorobiaceae (Fig. 8), are mostly smaller than of those utilizing the common enzymatic carboxylations [45,46]. The isotopically lightest organic carbon hitherto encountered in the terrestrial biosphere has been furnished by methanotrophic bacteria, with δ13C values of about –80‰ in specific metabolites [47]. Apart from these extremes, Summons et al. [48] have shown that type I methanotrophs utilizing the ribulose monophosphate cycle (Table 1) yield negative fractionations between 16 and ~30‰ in the synthesized biomass, while Zyakun and Zakharchenko [49] have reported corresponding fractionations between 10 and 34‰ for methanotrophs in general. Assuming a methane substrate with δ13C around –20‰, such fractionations would give rise to organic carbon with a δ13C-range from roughly –30 to between –50 and –60‰. Apart from fractionations inherent in the assimilatory pathways, enzymatic decarboxylations and related dissimilatory processes (Fig. 7, k4) may also contribute to the overall isotopic composition notably of higher plants. Although conflicting results have been reported with regard to the magnitude and even the direction of the isotope effects inherent in these processes, in vivo decarboxylations appear to release CO2 that is isotopically lighter than the parent organic material [39] with isotope fractionations thus running counter to those of the assimilatory pathway. Most probably, discrepancies between fractionations predicted by the isotope discriminating properties of specific enzymes and those actually observed can be ascribed to the antagonistic effect of respiratory decarboxylations. It is well known that photorespiration is particularly pronounced in C3 species due to the oxygenase activity of RuBP carboxylase, this also places limits on the productivity of C3 plants [42]. Figure 8 summarizes the net results of the interplay of these various fractionation processes in the form of observed δ13Corg spreads for the principal groups of extant higher

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plants, eukaryotic algae, and photosynthetic and chemosynthetic bacteria. The fractionations expressed by these ranges are gross fractionations as defined by Eq. (2). It can be inferred from this compilation that, depending on which of the isotope-discriminating steps shown in Fig. 7, and/or which of the carbon-fixing reactions listed in Table 1 become ratecontrolling in the specific instance, the isotopic composition of plants and microorganisms may vary over an extended range. A detailed and fully referenced discussion of the individual isotope distribution patterns represented in Fig. 8 has been given elsewhere [35,40,50–52]. Since the C4 dicarboxylic acid pathway is a late achievement in the evolution of flowering plants (angiosperms) not predating the onset of the Cretaceous (~130 million years ago), the impact of C4 photosynthesis on the long-term geochemical carbon cycle has been, as yet, negligible. Occurrences, in the present world, of C4 and CAM species are limited or at best moderate, with the C4 species primarily represented by tropical grasses and the CAM species, by succulent plants. If weighted for their relative contributions to the contemporary standing biomass, the isotope spreads of the principal groups of primary producers presented in Fig. 8 would indicate that the δ13C values of the global biomass are, on average, between 20 and 30‰ more negative than those of oceanic bicarbonate, the most abundant inorganic carbon species in the surficial environment. It should be noted that this conspicuous enrichment of 12C in organic matter derives, for the most part, from the isotope-discriminating properties of RuBP carboxylase, the key enzyme of the Calvin cycle. Being responsible for the bulk of the carbon transfer from the nonliving to the living realm, the RuBP carboxylase reaction was bound to impose its isotopic signature on the terrestrial biosphere as a whole, imparting to it a main δ13C range of about –26±7‰ [35,53]. 2.2.2.2. 13C/12C in Sedimentary Organic Carbon: Index of Biological Carbon Fixation The isotopic difference established between biogenic (organic) and inorganic carbon in Earth’s surficial environment (Fig. 8) is basically preserved when organic carbon and carbonate enter newly formed sediments. In fact, the glaring preference for 12C evident in fossil organic matter appears to be one of the most tenacious and durable relics of the ordered state of the biological precursor substances that is retained in sedimentary organics over billions of years. Although diagenetic alteration in the sediment has been shown to cause discrete secondary shifts in the original isotopic composition of organic materials, such alterations are usually small, hardly exceeding 2–3‰ in the case of diagenetically mature kerogenous substances [35,52,53]. Also, in the case of carbonate, secondary changes in the carbon isotopic composition over the diagenetic pathway from the parent carbonate mud to the solid carbonate rock tend to stay well below 2‰. Kerogenous substances with biogenic 13C/12C signatures and their graphitic derivatives can actually be traced back to the very beginning of the record, ~3.8 Ga ago, in sedimentary rocks [53–56]. Figure 9 provides convincing testimony that the carbon isotope spreads of extant primary producers or autotrophs have been summarily transcribed into the geological record with just the extremes truncated, indicating that the effect of a later diagenetic overprint of the primary 13C/12C ratios is indeed rather limited and, for the most part, gets lost within the broad scatter of the original values. The principal message conveyed by the broad envelope of δ13Corg values shown in Fig. 9 is, therefore, that the kinetic isotope effect that governs photosynthetic carbon fixation has been continuously propagated from the surficial environment into the rock section of the carbon cycle since early geological times. With this established, there can be little doubt that the conspicuous 12C enrichment displayed by the data envelope for fossil organic carbon presented in Fig. 9 constitutes a coherent isotopic signal of autotrophic carbon fixation over ~4 Ga of recorded Earth history as it ultimately rests with the process that gave rise to the biological precursor materials. Moreover, the long-term uniformity of the signal attests to an extreme degree of conserva-

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Figure 9. Isotope age functions of organic carbon (Corg) and carbonate carbon (Ccarb) as compared with the isotopic compositions of their progenitor substances in the present environment (marine bicarbonate and biogenic matter of various parentage, cf. right box). Note that the δ13Corg spread of the extantbiomass is basically transcribed into recent marine sediments and the subsequent record back to 3.8 Ga, with the Isua values reset by amphibolite-grade metamorphism. In the displaced Isua segment, the lower shaded portion represents the range of values with bona fide biological signatures (δ13Corg<–16‰) that have ostensibly survived the metamorphic reconstitution of their host rock; the upper light field covers those values, which, for the most part, have suffered a shift in positive direction as a result of high-T 13C/12C exchange. Superimposed on the Isua envelope for whole-rock analyses are the spreads obtained for carbon inclusions in apatite grains from the purportedly 3.85-Ga-old neighboring Akilia banded iron formation (A1) and from several Isua ironformations (A2) as reported by Mojzsis et al. [55]. The envelope for fossil organic carbon as a whole is an update of the database presented by Schidlowski et al. [35], comprising the means of some 150 Precambrian kerogen provinces as well as the currently available information on the Phanerozoic record. The negative spikes at 2.7 and 2.1 Ga indicate a large-scale involvement of methane in the formation of the respective kerogen precursors. Contributors to the contemporary biomass are (1) C3 plants, (2) C4 plants, (3) CAM plants, (4) eukaryotic algae, (5a, b) natural and cultured cyanobacteria, (6) groups of photosynthetic bacteria other than cyanobacteria, (7) methanogenic bacteria, and (8) methanotrophic bacteria. The δ13Corg range in recent marine sediments [57] is based on some 1,600 data points (black insert covers >90% of the database).

tism of the basic biochemical mechanisms of carbon fixation. In fact, the mainstream of the envelope for δ13Corg can be most readily explained as the geochemical manifestation of the isotope-discriminating properties of one, single enzyme, namely, RuBP carboxylase, the key enzyme of the Calvin cycle. As pointed out above, the carbon transfer from the inorganic to the organic world largely proceeds via the RuBP carboxylase reaction that feeds CO2 directly into the Calvin cycle as a 3-carbon compound (phosphoglycerate). As a result, the bulk of Earth’s biomass, both extant and fossil, bears the isotopic signature of C3 or Calvin cycle photosynthesis characterized by the sizeable fractionations of the RuBP carboxylase reaction that assigns a mean δ13Corg range of –26±7‰ to most biogenic matter. Occasional negative offshoots from this long-term average are commonly restricted to the Precambrian. There is no doubt that the conspicuous occurrences of super light δ13Corg values with extremes between –50 and –60‰ as documented by the Fortescue [35,53], and Francevillian anomalies [58] at about 2.7 and 2.0 Ga ago, respectively (Fig. 9), suggest a large-scale involvement of methanotrophic pathways in the formation of the respective kerogen precursors, which were ostensibly derived from isotopically light, 12C-enriched, microbial biomass. Whereas, at first sight, these excursions might appear as oddities confined to side stages of the carbon cycle, a closer scrutiny of Fig. 9 reveals that the respective

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negative extremes are superimposed on a markedly lowered margin of the δ13Corg envelope that characterizes the early Paleoproterozoic and Archean record as a whole [59,60] with δ13Corg means well below –30‰. Such increased fractionations may be most plausibly explained by the assumption that biogenic matter synthesized in common photosynthetic pathways (notably by RuBP carboxylase-based Calvin cycle photosynthesis) was remineralized by methanogens, with subsequent metabolizing of the isotopically light biogenic methane by methanotrophic bacteria [61,62] giving rise to exceptionally 12C-enriched organic matter. Altogether, these findings are likely to attest to an important role of methane in biogeochemical carbon transformations on the early Earth. Another peculiar feature of the carbon isotope age functions represented in Fig. 9 is an apparent discontinuity ~3.5 Ga ago between the main body of the database and the oldest record that is basically represented by the metasedimentary suite of the Isua Supracrustal Belt of West Greenland. While the average isotopic composition of sedimentary organic carbon over the last 3.5 Ga (δ13Corg= –26±7‰) can be taken as conclusive evidence of a biological pedigree, the remarkable shift of this mean in a positive direction (δ13Corg= –13.0±4.9‰) in the Isua kerogens and their graphitic derivatives [53,54] had occasionally raised doubts whether or not values in this range constituted equally unequivocal indicators of biogenicity. Moreover, there is also a minor negative shift of 2–3‰ in the Isua carbonates as compared to the preceding record (Fig. 9). As is currently known, the record of unaltered sedimentary rocks holds out to 3.5 Ga. Older rocks are exceptionally rare and invariably bear a metamorphic overprint that was apt to gravely impair the biogeochemical and isotopic information encoded in the precursor lithologies. In essence, this oldest part of the record is represented by the Early Archean Isua suite, the most ancient greenstone-belt-type volcano-sedimentary succession currently known, with a maximum age either short of or around 3.8 Ga [63–65]. Apart from widespread metasomatism, the Isua rocks have experienced high-T (450–650 ˚C) metamorphism of upper greenschist to amphibolite facies [66,67]. Ever since the accumulation of the first comprehensive sets of Isua data [35,53,54] and early proposals that the Isua values had been reset by high-T isotopic reequilibration between coexisting organic and carbonate carbon in response to the metamorphic reconstitution of the host rock [35,54], a whole critical industry sprang up around the subject. Nevertheless, the original interpretation was subsequently borne out by a wealth of corroborative evidence. Both currently available thermodynamic data on 13C/12C exchange [68,69] and observations from a fair number of geologically younger metamorphic provinces [70–74] lend support to the notion that the present Isua anomaly is evidently due to a metamorphic overprint (Fig. 10). Therefore, it may reasonably be inferred that the normal δ13Corg and δ13Ccarb age functions had originally held out to ~3.8 Ga before obtaining their present forms in the wake of the metamorphic reconstitution of the Isua suite. Early criticism of this reequilibration concept had notoriously ignored the fact that chemical reactions in metamorphic systems are not subject to chaos but are governed by well-constrained physicochemical equilibria. It is, meanwhile, firmly established that 13 12 C/ C exchange can occur in kerogenous and graphitic rock constituents during both amphibolite and granulite facies metamorphism, provided there is a second carbon partner (in the form of either CO2-bearing fluids or carbonate susceptible to metamorphic decarbonation reactions). The gaseous-CO2 phase present in the metamorphic fluids constitutes an effective vehicle for carbon isotope exchange. Sometimes complete reequilibration may be achieved in the reduced carbon constituents, but, often, the exchange is only partial due to sluggish reaction kinetics. In any case, thermodynamic equilibria predict that 13C/12C ratios in kerogen and graphite increase during this process. Hence, high-T exchange equilibria are bound to push δ13C in sedimentary organics up towards more positive values and never in negative direction. Thus, the lowermost values encountered in metamorphosed organics are

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Figure 10. Decrease of carbon isotope fractionations between sedimentary organic and carbonate carbon as a function of increasing metamorphic temperature. In metamorphosed lithologies, these fractionations are conventionally expressed as difference between the δ13C values of coexisting calcite (cc) and graphite (gr), i.e.: Δ(cc-gr)=δ13Ccc–δ13Cgr. Δ(cc-gr) values reported by several authors [70,71,73] from different metamorphic terrains are shown to scatter around both the function of thermodynamically calculated isotope equilibria by Bottinga [68] and an empirical fractionation curve by Wada and Suzuki [72] calibrated by dolomite-calcite solvus temperatures. Note the conspicuous reduction of the scatter field at higher temperatures, but also that markedly discordant values can persist up to 600–650 ˚C, indicating that isotopic reequilibration between the two carbon species may be kinetically retarded even in the upper amphibolite facies.

always the least exchanged and most pristine [69]. Since the lowermost δ13C values of reduced (graphitic) carbon encountered in the early Isua surveys [53,54] had covered the range between –22 and –28‰ [PDB], this could be taken as straightforward evidence that carbon constituents with the isotopic composition of biogenic matter had been present in the pre-metamorphic Isua suite. More recently, this early interpretation was decidedly confirmed by the recovery of apparently pristine δ13Corg values from several banded iron formations of both the Isua Supracrustal Belt and the adjacent coeval Akilia suite, with results ranging from –21 to –49‰ [55], which clearly fall into the biological range. The values were recovered from miniscule carbon inclusions in single apatite grains, utilizing the latest techniques of ion microprobe microanalysis. In this particular case, carbonaceous material sealed in a mineral matrix and hosted by a carbonate-free lithology had obviously escaped high-T isotope exchange, thereby preserving its original biogenic δ13Corg spread with, probably, little alteration. The remarkably negative δ13Corg mean of –37±3‰ displayed by the apatite-hosted carbon particles certainly conjures up a methane connection for sedimentary organic carbon accumulated during Earth’s early history [61]. Altogether, the isotope data obtained for these apatite-coated carbon blobs confirm the presence, within the Isua sediments, of reduced carbon constituents that bear the isotopic signature of life processes, with the suspected biological linkage further supported by the conspicuous carbon-phosphate connection. Also, Rosing [75] has lately submitted another set of δ13Corg values retrieved from various carbonbearing Isua lithologies, whose spread (–11.4 to –20.2‰) falls well into the range observed in the early pioneering studies [54]. Starting with relevant considerations by Nagy et al. [76], opinions have been occasionally voiced that the graphite content of the Isua metasediments might have originated from inorganic processes, such as a high-T oxidation of methane (CH4) by ferric iron oxides or CO2, by reduction of carbon dioxide by ferrous iron minerals, or by thermal decomposition of iron carbonate (siderite, FeCO3) with a concomitant disproportionation of carbon to give CO2 and graphite [77–79]. While, particularly, the last process cannot be excluded for the origin of some finely dispersed graphite particles within the secondary (metasomatic) carbonate members of the suite that show evidence of fluid infiltration and a concomitant

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hydrothermal overprint, such interpretation can safely be discarded in the case of the more conspicuous bedded streaks and accumulations of graphitic material, which conform with the typical stratiform nature of common sedimentary organics. Particularly, it is this close alignment of the organic component with recognizable sedimentary features that militates against attempts to invoke another pedigree for the bulk of the reduced carbon constituents from the Isua metasediments than for their counterparts in the preceding unmetamorphosed record. It is well known that the oldest unmetamorphosed sediments from the time window 3.2–3.5 Ga ago contain appreciable quantities of kerogenous carbon [53,80,81]. Since the Isua supracrustals are metamorphic derivatives of genuine sediments [82], the Isua suite would figure as the only sedimentary sequence in the whole record lacking an indigenous organic carbon component if the reduced (graphitic) carbon constituents of the present rocks were supplied by inorganic sources. the identification of a possibly inorganic graphite component within the Isua suite seems to call for differential diagnostics applying both meticulous microfabric and microchemical analysis. Moreover, comparative studies of metamorphosed carbonate sequences bearing a strong metasomatic and/or hydrothermal overprint from geologically younger formations, where contemporaneous biological activity can be taken for granted, might be helpful to provide a baseline for a judicious evaluation of relevant Isua data. Altogether, to invalidate a biological interpretation of the Early Archean δ13Corg record, an inorganic process capable of mimicking, both in direction and magnitude, the principal enzymatic isotope effect of the photosynthetic pathway with a remarkable degree of precision would have to be postulated. With a convincing alternative as yet missing and an early emergence of life on the juvenile planet suggested by independent data, the balance of the currently available evidence is decidedly consistent with the notion that biologically mediated carbon isotope fractionations have persisted over 3.5 Ga, if not 3.8 Ga, of geological history. Accordingly, the mainstream of the δ13Corg age function depicted in Fig. 9 may be aptly termed an index line of autotrophic carbon fixation over the hitherto known sedimentary record. 2.2.3. Molecular Biomarkers (Chemical Fossils) The term molecular biomarker refers to a variety of discrete organic compounds or molecular structures that are evidently derived from living organisms and have come to be stored in sedimentary rocks. Representing chemical analogues of morphologically preserved relics of former plants and animals, these molecules are known also as chemical fossils [83,84]. Apparently, a fair number of chemically stable, refractory molecular structures of biological pedigree have an inherent capability to survive the wholesale breakdown of organic matter after burial in sediments (Fig. 6) and the even harsher conditions during the metamorphic reconstitution of their host rock with relatively little impairment. Some of these compounds have demonstrably preserved their structural and stereochemical identity (albeit sometimes severely mutilated) since Archean times, giving eloquent testimony that the enzymatic machinery responsible for their biosynthetic generation has worked virtually unchanged over billions of years. As a result of the pioneering work by Treibs [85], organic pigments, such as porphyrins, were the first compounds to be identified as authentic chemical fossils in a variety of ancient organic materials. The tetrapyrrole ring of the porphyrine structure enclosing a central metal ion constitutes a very peculiar molecular architecture that forms the backbone of the chlorophyll and heme molecule, which principally differ by the occupation by either Mg or Fe as the central metal position. Chlorophyll contains, furthermore, a characteristic side chain (Fig. 11) that commonly breaks off from the main ring structure during diagenesis, furnishing alternatively, two different isoprenoid hydrocarbon chains, phytane and pristine, whose relative proportions may vary as a function of the diagenetic environment. Diage-

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Figure 11. The chlorophyll structure as a prototype of a biochemical marker molecule. During diagenetic alteration in sediments, the tetrapyrrole ring is transformed into a porphyrin complex with an exchange of the primary Mg constituent by other metals, such as V). The lateral phytyl chain gives rise to, alternatively, two isoprenoid hydrocarbons, phytane and pristane. The isoprenoid chains usually break away from the main ring structure and figure as separate biomarker molecules.

netic alteration of the main body of the porphyrine ring commonly results in an exchange of the primary metals, Mg and Fe, by a whole array of secondary metals among which V and Cu are fairly prominent. Chlorophyll and heme derivatives in the form of porphyrins and isoprenoid fragments, phytane and pristine, were shown to be ubiquitous in most sedimentary organics inclusive of oils [86], with phytane and pristane separately attesting to the presence of former biosynthetic activity. Another outstanding molecular biomarker is cholesterol, a sterol widely distributed in all eukaryotic organisms and characterized by a highly ordered carbon skeleton with a peculiar stereochemistry. The stereochemical setup comprises, inter alia, eight chiral centers, which impart a high degree of intramolecular complexity to the cholesterol structure that is additionally enhanced by the specific carbon isotope preferences exercised by each of these centers. With these characteristics, cholesterol qualifies as the very paragon of a molecular fossil. Mention should be made that specific sterol derivatives, namely, 28- to 30-carbon steranes, have been recently reported from 2.7-Ga-old shales of the Hamersley Basin, Australia [87]. Since no prokaryotes have been shown to produce the type of elaborate sterol precursors of steranes with such high carbon numbers, it must necessarily be accepted that biochemical evidence of eukaryotic physiology dates back in the record to Late Archean times, which suggests that the emergence of the eukaryotic cell occurred much earlier than hitherto accepted. A further group of biomarker molecules that have recently come into focus are 2-methylhopanoids [88]. These are highly refractory pentacyclic triterpane hydrocarbons resulting from the degradation of a specific group of lipids that are profusely synthesized in the membranes of cyanobacteria, where they exercise the same regulating and rigidifying function that is served by sterols in all higher (eukaryotic) forms of life. Of late, cyanobacterial-specific chemofossils of this affinity, 2α-methylhopanes, have been extracted abundantly from 2.7-Ga-old sediments of the Australian Hamersley Basin [87], which constitutes corroborative biogeochemical evidence for the extreme antiquity of cyanobacteria suggested by other lines of evidence. 3. Summary and Outlook Accepting a cosmic universality of biological principles in analogy to the proven universality of the laws of physics and chemistry, it must necessarily be postulated that the fossil

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manifestations of life as observed in the oldest terrestrial sediments constitute analogues of possible counterparts in extraterrestrial settings, notably, from early Martian formations. This should hold for both the morphological, cellular and biosedimentary, relics and the biogeochemical residues of former organisms which, with their inherent preservation potential, would qualify for entry into the sedimentary record of any life-hosting planetary body. Fossilization scenarios of such a kind may be specifically envisaged for the sedimentary formations deposited during the water-rich period in the early history of Mars. As is generally accepted, the stratified rock formations exposed on large parts of the Martian surface, such as in the Tharsis region and the associated Valles Marineris canyon system, represent well-bedded sediments believed to include, inter alia, thick carbonate sequences [7]. Since these sediments were obviously formed in an aqueous environment conducive to the initiation and maintenance of biological processes [89], the presence of contemporaneous Martian life comparable to that on the Archean Earth should be predictably documented in these rocks in the form of micropaleontological and biogeochemical (inclusive of isotopic) evidence. For the evaluation of such exotic paleobiological inventories whose possible existence is suggested by several lines of evidence recently set out by McKay et al. [90] and Gibson et al. [91], the terrestrial record provides a crucial informational baseline. Considering the ubiquity of fossil organic carbon in the terrestrial rock record compared to the scarcity of morphological fossils, biogeochemical evidence is likely to play a key role in any future search for past life in extraterrestrial materials. Specifically, the identification in Martian sediments of 13C/12C fractionations between carbonate and reduced carbon similar in direction and magnitude to those observed in the terrestrial record could be taken as a strong indication for the involvement of life processes in the carbon isotope systematics of such formations. While carbon isotope fractionations hitherto reported from SNC meteorites [92] representing sputtered Martian crust may suggest a biological linkage, the general petrography of the material and other imponderabilities surrounding the samples render conclusions based on rocks decidedly less authentic than those that might be ultimately derived from an analysis of genuine Martian sediments. In any case, there is reason to believe that the kinetic isotope effects besetting enzymatically mediated carboxylation reactions are not confined to the common brand of earthly biochemistry, but should abound in exobiological systems as well [93]. Since carbon isotopes had allowed first powerful inferences on the antiquity of terrestrial life at a time when the paleontological record for the Archean was either deplorably scanty or altogether missing [94,95], it may be safely assumed that the predictive power of 13C/12C ratios in corresponding extraterrestrial settings should not, by any means, be inferior to those displayed on Earth. Hence, even a modest body of carbon isotope data retrieved from bona fide Martian sediments might furnish crucial constraints for current discussions on the existence of former and possibly extinct life on Mars [93,96]. According to a well-known dictum by Louis Pasteur, only the “prepared mind” is apt to make those discoveries that are incumbent, and ostensibly due, at a certain stage of scientific and technological evolution. To create this kind of preparedness in the search for fossil manifestations of extraterrestrial life, the evidence furnished by the oldest geological record plays a crucial role since it is bound to sensitize potential investigators to the subject in the widest sense.

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Formation of Ordered Structures of Charged Grains in Gas-Dusty Atmospheres of Planets and Comets during Lightning Discharge Yuriy G. SEROZHKIN Arsenal Central Design Bureau, Kiev, Ukraine Abstract. The electric discharges in gas-dusty atmospheres—the atmosphere of earlier Earth, the atmosphere of comets, and dust storms on Mars—can serve not only as an energy source for the formation of composite organic compounds, but also, in the case of gas-dusty atmospheres in dusty plasma of electric discharges, the formation of ordered structures of charged dust components is also possible. The dusty plasma with a high electronic temperature passes into a plasma-crystalline state with particular restrictions of initial scatter of grain velocities in a wide enough pressure range of gas component and discharge parameters. During these discharges, micronsized particles can be charged up to magnitudes of 104 of the elementary charge. These particles interact with the discharge plasma and form ordered structures. Scatter of particle velocities, at which this may occur, suggests the atmosphere of comets, 1 cm s–1; high layers of an Earth’s atmosphere, 100 cm s–1; and dust devils on Mars, 250 cm s–1.

Introduction Understanding the transition from chemical evolution to biological evolution is one of the most intriguing tasks of modern astrobiology. Even the statement of the question is not clear. Development of models or self-organization in which formation of prebiological compounds occurs on crystal or colloid structures, such as on a template, is one direction to search for ways of stating and answering this question [1,2]. Ordered structures (dustplasma crystals) that form under certain conditions in dusty plasmas are of extreme interest to researchers in this context. Research has been carried out in a range of pressure from 1 atm to 0.01 torr, concentrations of dust ranging from 102 to 106 cm–3, and sizes of grains from 0.1 to 25 µm [3–7]. The similar properties of dusty plasma in comparison with results obtained by the synthesis of organic compounds through electric discharge should attract research attention when attempting to understand the formation of prebiotic compounds and structures in dusty plasmas. The plasma of lightning discharge in gas-dusty atmospheres of some bodies in the solar system can be an ideal medium for the formation of ordered structures and, at the same time, be a medium for the synthesis of complex organic compounds. The real role of electric discharges during the synthesis of prebiological systems is not clear and is considered rather skeptically. The discharges used in experiments on the synthesis of organic substances do not even remotely resemble the discharges observable in nature. Another aspect of the role of electric discharges in the formation of prebiotic condi-

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Table 1.

tions on Earth is connected with thunderstorm activities in the modern atmosphere and is interlinked to the presence of ice crystals in an atmosphere. Determining the degree of thunderstorm activity in early Earth environments, during the period when conditions of prebiotic synthesis prevailed, is difficult. At the same time on Earth and possibly on other bodies in the solar system, there are conditions in which discharges occur without the participation of ice crystals. The carriers of charges in this case appear to be dusty grains. The possibility of detecting electrical activity in dust storms on Mars is considered in several publications [8–10]. The author suggested that early work should include surveys of conditions where the development of electric discharges is possible in near-surface gas-dusty atmospheres of comets [11,12]. For an estimation of discharge parameters, possibly occurring in gas-dusty atmospheres of Mars or comets, results of research on discharges (sprites) in the high layers of Earth’s atmosphere are considered [14,15]. The discharges of this type occur at altitudes 50–100 km above regions of thunderstorm concentrations. The parameters of the atmosphere at these altitudes are between conditions existing in the Mars atmosphere and atmospheres of comets.

1. The Characteristics of Gas-Dusty Atmospheres and Dusty Plasma of Discharges The electrical activity in a gas-dusty atmosphere is determined by values of electrical fields, charges that accumulated on a dust component, pressure of gas, and concentration and properties of the dust components. A dust component in the broadest sense of the term is a not only a gaseous component atmosphere, particularly crystals of ice in thunderstorm clouds, but it is also possible to consider dust components. Until now there has been no conventional theory explaining the processes of electrification of drops of water, ice crystals, and dust. It should be noted only that the progress in understanding the macrophysics of processes of electrification will be connected to the study of processes in dusty plasma [16]. The parameter data of gas-dusty atmospheres and the electrical fields in them, taken from the above-mentioned papers, are shown in Table 1. Micron-sized particles can not accumulate a charge up to values of several units of an elementary charge due to Coulomb force repulsion under usual conditions. However, they can be charged up to values Zd=103–105 elementary charge in lightning discharges by adhering electrons to them with temperature Te=1eV. The maximum charge of a particle is determined by cathode rays and ions (quantity in units of time) on a surface negatively charged particle [6,7]. The author has estimated that in discharge plasmas in the considered atmospheres, there are conditions for the charging of micron-sized particles up to Zd=1×104 [12,13]. Based on the atmospheric parameter data, the characteristics of dust plasma necessary for an estimation of conditions for formation of ordered structures will be determined. Parameters of concern are temperature of electrons, Te, and ions, Ti; mean velocity of electrons, ve, and ions, vi; drift velocity of electrons vDe, concentration of electrons, ne, and ions, ni, and plasma frequencies of electrons, ωpe, ions, ωpi, and charged dust

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Table 2.

components, ωpd. Approximations and assumptions on which the evaluations are made can be found in earlier work [12,13], and the results of evaluations are shown in Table 2. Further, the possibility of formation of ordered-structure charged micron-sized particles in all three atmospheres will be estimated.

2. Formation of Ordered Structures of Charged Microparticles Two requirements for the formation of ordered structures include: (1) the presence of attractive forces and repulsion between components and (2) an effective mechanism for equalization of velocities or a mechanism for cooling. As shown in several publications [4,5] on dusty plasmas, in an open system, there are padding attractive forces and repulsions between charged dusty particles. Under certain conditions, these give rise to instabilities of self-compression and lead to the collapse of dust clouds. For the analysis of these requirements the following dimensionless parameters will normally be used:

P = (Z d × n d ) / n e , τ = Ti / Te ,

(1)

where P shows a part of negative charge on dust particles in relation to the electron concentration and τ is the relation of ionic and electronic temperatures. Goree et al. [4,5] showed that for P = 10 and τ = 1 there are ranges of values of parameters for dusty plasma, from which the processes of self-compressions being in an incipient state of dusty plasma crystal formation can be deduced. That τ = 1, is obvious and it can be seen from the data given in Table 2 that the considered objects satisfy the condition P ≈ 10. The so-called parameter of degree of Coulomb interlinking, Gc, is a criterion of the formation of ordered structures in dusty plasma. It is determined as the relation of a potential energy of interaction of charged particles to a kinetic energy of particles in a center-of-mass system of dust particles:

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1 (Z d × e ) , kTd 4∂ε 0 L

173

2

Gc =

(2)

where k represents the Boltzmann constant, Td is the kinetic temperature of dust particles, Zd×e is the charge of dust particles, and L is the distance between particles. If this parameter is on the order of 2, the particle system behaves as a Coulomb fluid, and if the parameter is more 200, it is possible to consider a Coulomb crystal [6,7]. For example, the estimation of the requirement of temperature of micron-sized particles with a concentration of 103 cm–3 (the atmosphere of comets) and a charge of Zd×e = 104 for transition in a condition of a Coulomb liquid indicates Td ≤ 10–10 erg, which corresponds to speed vd ≤ 10 cm s–1. For the beginning of transition in a condition dusty-plasma crystal, it is necessary to reduce the speed to vd ≤ 1 cm s–1. In the atmosphere of Mars with concentration of particles 105 cm–3, the appropriate speeds are found to be in the range of 30 and 3 cm s–1. Friction in a neutral gas serves as the natural mechanism for cooling dust particles. Other mechanisms for cooling, such as interaction between charged dust particles and radiation of collective plasma modes (the dust sound), in a number of cases can exceed cooling caused by friction in a neutral gas. The conditions of dust-sound radiation and the degree of cooling of particles by radiation are considered by Goree et al. and Tsytovich and Resendes [4,5]. These articles note that this mechanism for cooling works in the absence of neutral gas and its effectiveness is incremented in dusty plasmas with a high electronic temperature, and it corresponds to dusty plasma at the discharge of lightning in an atmosphere of comets. The requirement of the existence of a dust sound has the following form [4]: ⎛ n ⎞ Td << Ti Z d ⎜⎜ Z d d ⎟⎟ . ni ⎠ ⎝

(3)

Conditions of the existence of a dust sound in the considered atmospheres are estimated using values listed in Table 2. For the atmosphere of a comet, Td<<2×10–7 erg will be used. A particle mass of 2×10–12 g corresponds to a velocity of vd <<2×102 cm s–1. In the case of the Martian atmosphere, Td<<1.6×10–9 erg. At a particle mass of 4×10–12 g, it corresponds to a velocity of vd <<30 cm s–1. For the high layers of Earth’s atmosphere, the requirement will be the same, as well as for dust storms on Mars. An estimation can be made of the velocity of energy loss by a particle because of the radiation of a dust sound. According to Goree et al. [4], (dTd/dt)ds is described by the formula 45π ⎛ dTd ⎞ ω pd z i 3 Ti n i a 3 ⎟ =− ⎜ 4 ⎝ dt ⎠ ds

(

)⎛⎜⎜ n nZ i

⎝

d

d

⎞ ⎟⎟ , ⎠

(4)

where Zi = (Zde2/aTi). For a comet atmosphere, dTd/dt ≈ 1×10–10 erg s–1; for a Martian dust storm, dTd/dt ≈ 7×10–5 erg s–1; and for the high layers of Earth’s atmosphere, dTd/dt ≈ 2×10–6 erg s–1. The value of the energy loss is determined by the lifetime of an ionic cloud and in turn primarily depends on transversal diffusion of ions. This lifetime is approximately determined by a ratio of velocities of the electronic and ionic component. It is possible to consider that this time is ~10 ms for comets and Earth while, for Mars, it is ~1 ms. From Eq. (4), it follows that the energy loss due to radiation of a dust sound does not depend on the velocity of particles. At a time of 10 ms, the particle in a comet’s atmosphere will lose energy at dTd ≈ 1×10–12 erg because of radiation of a dust sound. At a velocity of vd ≈ 1 cm s–1, the corresponding change of velocity is ∆vd ≈ 1 cm s–1, i.e.: full loss of veloc-

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ity. In Earth’s atmosphere, these losses will result in the value dTd ≈ 2×10–8 erg. It corresponds to full loss of velocity at vd = 100 cm s–1. In a dust storm in the Martian atmosphere, dTd ≈ 7×10–8 erg, which corresponds to a velocity loss of 250 cm s–1. In the two last cases, the value of energy loss is greater than the values of energy of particles at which the existence of a dust sound is possible. This means that the radiation of a dust sound will cause cooling of dust components. Thus, the executed estimation shows that, under the gas-dusty atmosphere conditions considered under certain parameters, there is a capability for the formation of ordered structures of charged micron-sized particles. Can such structures claim a role as matrices for formation of prebiological compounds? First, the answer to this question depends on the presence of the charged grains changing conditions supporting synthesis of composite organic compounds. It would be extremely interesting to pull together laboratory research of the process of formation of organic compounds under the effect of electric discharges with real conditions present in the solar system. When reconstructing conditions in which there could be a change from chemical evolution to biological evolution, it is necessary to take into account the fact that most bodies in the solar system have gas-dusty atmospheres. Research of the synthesis of organic compounds in dusty plasmas with discharges would result in additional understanding of processes of formation and self-organization of prebiological compounds.

References [1] Bernal JD. The origin of life. London, 1967. [2] Carins-Smith AG. The first organisms. Sci. Am. 1985 June; 252(6). [3] Thomas HM, Morfill G, Demmel V, Goree J, Feuerbacher B, and Möhlmann D. Plasma crystal: coulomb crystallization in a dusty plasma. Phys. Rev. Lett. 1994; 73: 652–5. [4] Goree JA, Morfill G, Tsytovich VN. Excitation of collective plasma modes during collisions between dust plasma crystals. Plasma Phys. Rep. 1998; 24 (6): 534–41. [5] Tsytovich VN, and Resendes D. Dispersive properties and attraction instability of low-frequency collective modes in dusty plasmas. Plasma Phys. Rep. 1998; 24(1): 71–82. [6] Belotzerckowsky OM, Zacharov IE, Nefedov AP, Sinkevitch OA, Filinov VS, Fortov VE. Effective potential of interaction. J. Experimental and Theoretical Phys. 1999; 115(3): 819–36. [7] Ivanov VV, Pal AF, Rachimova TV, Serov AO, Suetin NV. Influence of dusty component. J. Experimental and Theoretical Phys. 1999; 115(6): 2020–36. [8] Farrell WM, Keiser ML, Desch MD, Houser JG, Cummer SA, Wilt DM, Landis, GA. Detecting electrical activity from Martian dust storms. J. Geophys. Res. 1999 February 25; 104(20): 3795–801. [9] Levin Z, et al. Lightning generation in planetary atmospheres. Icarus 1983; 56(80). [10] Eden HF, Vonnegut B. Electrical breakdown caused by dust motion in low-pressure atmosphere: consideration for Mars. Nature 1979; 280: 962. [11] Serezhkin YuG. Lightning in the atmosphere of a comet and the origins of prebiological systems. Proceedings of SPIE 2000; 3755: 242–50. [12] Serezhkin YuG. Formation of ordered structures of charged microparticles in near-surface cometary gasdusty atmosphere. Proceedings of SPIE 2000; 4137: 1–12. [13] Serezhkin YuG. Gas-dusty atmosphere near the surface of Mars, comets and high layers of Earth’s atmosphere as a medium of formation ordered structures from charged microparticles. Proceedings of SPIE 2001; 4495: 223–34. [14] Pasko VP, Inan US, Bell TF, Taranenko YN. Sprites produced by quasi-electrostatic heating. J. Geophys. Res. 1997 March 1; 102(A3):4529–61. [15] Gerken EA, Inan US, Barrington-Leigh CP, Telescopic imaging of sprites. Geophys. Res. Lett. 2000 September 1; 27(17):2637–40. [16] Mareev EA, Sorokin AE, Trakhtengerts YV. Effects of collective charging. Plasma Phys. Rep. 1999; 25(3): 289–300. [17] Smirnov VV. Electric fields of dust streams. Izvestia An. Phys. of Atm. and Ocean 1999; 35(5): 616–23.

Perspectives in Astrobiology R.B. Hoover et al. (Eds.) IOS Press, 2005 © 2005 IOS Press. All rights reserved.

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Exobiology of Titan Michael B. SIMAKOV Group of Exobiology, Institute of Cytology RAS, Tikhoretsky Av., 4, St. Petersburg, 194064, Russia Abstract. Life depends on liquid water (H2O), a suite of biogenic elements (carbon (C), oxygen (O), nitrogen (N), sulfur (S), and phosphorous (P)), and a useful source of free energy. All these requirements are on Titan, the largest satellite of Saturn. An internal liquid ocean and a dense atmosphere determine a great exobiological significance of the satellite. The putative ocean may have a chemical composition useful to living organisms, which could maintain different biogeochemical cycles there.

1. Atmosphere Titan, the largest satellite of Saturn, has a great exobiological significance. Its dense atmosphere is composed primarily of N2 with ~8% methane (CH4) and has a large similarity to Earth’s primordial atmosphere. The existence of such a substantial atmosphere is an unresolved question today. The main attention from an exobiological point of view devotes itself to a very complex atmospheric chemistry. The interaction of ultraviolet (UV) light and cosmic rays with atmospheric constituents produces a complex ion chemistry, which leads to the formation of a large variety of massive ions and organic molecules. The main products of these reactions are different hydrocarbons, both saturated and unsaturated; nitriles; and other N-organics [1,2]. The dissociation of N2, coupled with photolysis of methane, form the basis for further chemical processes; the initial set of 47 reactions was given by Clarke and Ferris [3]. A large number of minor constituents in the gas and solid phases, such as carbon monoxide (CO), carbon dioxide (CO2), ethane, ethylene, acetylene, cyanoacetylene, hydrogen cyanide, and many others, were identified in the atmosphere with abundance ranges from 10–9 to 10–7. The atmosphere has at least three haze layers, which are also rich in organics. Titan’s organic haze is a potentially important sink of the photochemically produced carbon and nitrogen compounds. The complex organic mixture of simple alkane, aromatic compound, heteropolymer, and amino acid precursors forms tholins—the solid organic product with a very poorly known molecular composition. Analysis of the experimental tholins revealed more than 75 constituent compounds. The products of photolysis could cover the satellite’s surface with 100–200 m and more [4]. The oxygen-bearing compounds (CO, H2O, and CO2) from external and internal sources have recently been discovered on Titan, and these compounds can induce the production of several oxygenated compounds through energetic action.

2. Brief History of Titan Accretion models of the Saturnian satellite suggest that heating released during late stages of its formation was sufficient to create a warm, dense atmosphere with a mass at least 30

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times greater than the present value [5] and a large open ocean on its surface. Such a juvenile Titan ocean could exist during a period of 108 yr. Because the great part of the primordial Titan atmosphere could be supplied by comets during or after accretion [6], the composition of such an atmosphere would have mostly consisted of H2O, N2, CO, and CO2 since the cometary carbon appears concentrated in the form of CO (ranging from a few to 45%, relative to water), CO2 (~15%), and heavy organics [7,8]. The mass of volatiles acquired by Titan from comets would be expected to be about 1020 to 1022 g for CO and 1020 to 1021 g for nitrogen [9]. So, Titan’s primordial atmosphere could be warm, dense, and consist of CO2-(CO)-N2. Complex organic compounds may have also been acquired from cometary and chondritic material [10]. The first stages of chemical evolution would have taken place in that atmosphere and ocean under the action of such energy sources as ultraviolet radiation, solar wind, galactic cosmic rays, magnetospheric-plasma ion bombardment, electrical discharges, and radiogenic heat. Recent attempts to establish a lower limit for the time required for the emergence of life suggest that 10–100 Ma was enough in case of Earth [11], and the time of existence of Titan’s juvenile ocean was enough for the emergence of the first protoliving objects. As the planet developed, several energetic processes (irradiation, lightning, and meteoritic and comet impacts) produced different forms of fixed nitrogen. All nitrogen could have been in the fixed form at the end of the planetary accretion period. Such a scenario has been supposed by Mancinelli and McKay [12] for the evolution of prebiotic nitrogen cycling on Earth, and similar processes could be proposed in the case of the Saturn’s satellite. Hence, in the absence of a recycling mechanism, dissolved NO2– and NO3– would accumulate in the ocean. During the cooling phase, Titan’s ocean was covered with an icy crust. If life had originated by then, it could survive to the present in some places [13]. On Earth, microbial life exists in all locations where microbes can survive. On the other hand, the variety of prebiotic processes can take place on Titan at the present time. Many volatiles and inorganic salts were probably present in the primordial liquid layer, and they must decrease the freezing temperature of the liquid at the cooling stage. The compositions of the rich atmosphere, which is host to extensive organic photochemistry, and internal liquid layer must be very complex, and Titan’s putative ocean might harbor life or complex prebiotic structures. The most recent models of Titan’s interior lead to the conclusion that a substantial liquid layer exists today under a relatively thin ice cover [14–16]. Lunin [17] has shown that the underground ocean is the only structure that is consistent with all of the known constraints (chemical, tidal, ground-base radar, and near-infrared observation), and Lorenz [18] has found that internal oceans are mandated for the large icy satellites. Thermal evolution models also predict the existence of a thick (~300 km) liquid layer with a relatively thin (~80 km) ice cover [16]. Spohn and Schubert [19] have shown that even radiogenic heating in a chondritic core may suffice to maintain a liquid ocean inside large icy satellites.

3. The Possible Biogeochemical Cycles in the Water Layer The present composition of the putative liquid layers of the ice satellites is probably very complex. Mass balance calculations modeled on the extraction of elements from chondritic material into the aqueous phase [20] show that Titan’s extensive subsurface ocean is also likely to contain dissolved salts from endogenic materials that resemble carbonaceous chondrite rocks incorporated into the satellite during its formation and released at the time of planetary differentiation.

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There are three sources of organic carbon (Corg) for Titan’s ocean: (1) complex atmospheric chemistry, (2) carbonaceous chondrites and cometary bodies, (3) and sea-floor hydrothermal systems. Since the light energy in the form of the solar radiation is not accessible in such conditions (the solar flux to Titan’s surface is ~1.1% of Earth’s), chemical energy has to be the main source that drives life and other disequilibrium processes. So, the initial components, such as NO3, SO42–, CO32–, for the origin of lithoautotrophic processes could exist in Titan’s putative ocean from the earlier stages of the satellite’s evolution and provide biologically useful electron donor-acceptor pairs in the upper layer where the temperature and pressure are not very hostile. Nitrate accumulated in the ocean at the first stage of atmosphere’s evolution would have allowed the first protobiosystems to use it as the primary source of energy. It should be proposed that the idea that the first protoliving systems in Titan’s ocean could have had an internal energy source, namely, the chemical potential of an inorganic reaction or basic reaction (BR). There are some candidates on the role of BR. Electron acceptors, such as NO3–, SO42–, 3+ Fe , Mn4+, or CO2, have to be coupled with the electron donors. Electron donors that may be important in such process include H2, CO, CH4, Fe2+, Mn2+, pyrite, sulfur compounds, and organic material [21]. Some of these molecules could be generated abiotically on the bottom of the internal ocean by the reaction of water with rocks of the silicate mantle, by the reaction of water with meteoritic materials, and others could be synthesized under the action of radiation. A radiation-driven ecosystem has been proposed for Europa [22–24] and could work in the case of Titan. Four energetic full operative biogeochemical cycles are possible inside Titan’s ocean, namely, nitrogen (N-cycle), sulfur (S-cycle), iron (Fe-cycle) and carbon (C-cycle), and all of them could be connected each with each other [25]. BR of nitrate reduction to dinitrogen is more thermodynamically favorable in the row of different inorganic substrates [26]. The all-gaseous N in the contemporary Titan atmosphere could be the product of this reaction [27]. Very interesting bacteria, which use ammonium as an inorganic electron donor for denitrification, have been recently discovered [28]. This reaction has a very favorable energetic (–357 kJ/mol). Hydroxylamine (NH2OH) and hydrazine (N2H4) are formed as intermediates, and bicarbonate is the sole C source. This is the first case where hydrazine, a rocket fuel, is a free intermediate in any biological system. Both of these components could be widespread in Titan’s environments and could be used by microorganisms for energy transduction and the buildup of an electrochemical gradient. A start reaction can be hypothesized as N2H4→N2, which can evolve through NH2OH→N2H4→N2 to NO3–→NH2OH→N2H4→N2 at the route of microbial evolution. Dissimilatory ferric (Fe(III)) iron-reducing and ferrous (Fe(II)) iron-oxidizing organisms can also form the basis for a closed ecosystem, which gains energy through cyclic reduction and oxidation of iron minerals, sometimes by NO3–-dependent route. With H2S, inorganic sulfides [29], elemental sulfur, and various organic acids [30], Fe(III) oxyhydroxides are readily reduced. On Earth, microbial Fe(III) reduction is the major way of Corg oxidation in anaerobic environments [31]. Microorganisms utilizing Fe(III) as an electron acceptor were discovered in mesobiotic marine and freshwater anoxic sediments and submerged soils [32]. The denitrifying bacterium was isolated from the mud of the Mariana Trench [33], and it showed greater tolerance to low temperature and high hydrostatic pressure (50 MPa). Thermobiotic ecosystems also contain bacteria that are capable of reducing Fe(III) with formate, lactate, or molecular hydrogen. The production of reduced end products, e.g.: Fe(II), FeS by Fe-reduction, and H2S, with such processes could resupply BR with reagents. Ferrous iron is oxidized chemically by a number of inorganic compounds, most notably molecular oxygen, manganese oxide (MnO2), and nitrate, so a biogeochemical cycle for maintaining the primordial Titan ecosystem can be imagined. The putative life

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inside Titan does not depend on solar energy and photosynthesis for its primary energy supply, and it is essentially independent of the surface circumstances. There could be microorganisms having a great similarity with the last common ancestor on Earth. Rich chemosynthetic ecosystems could be associated with methane-clathrate areas on the icy bed. The cold methane vents induced by liquid methane could serve as a source for the formation of chemosynthetic ecosystems. These processes could involve a transfer of electrons from methane to sulfate or other electron acceptors. The examples of such systems could be found around methane clathrate on the Earth’s sea bed [34–35]. Some organisms are capable of disproportioning methanol, methylamines, or methyl sulphides to methane and carbon dioxide, oxidizing –CH3 groups to CO2 anaerobically. Microbial consortia based on anaerobic oxidation of methane coupled to sulfate reduction can support other microbial communities by generating a substantial biomass accumulation that is derived from methane [36]. Along with the upper layer of the internal, water ocean, when a temperature and pressure are suitable for living processes, there are some additional appropriate sites for biological and/or present day prebiological activity [37]: (1) water pockets and liquid veins inside the icy layer; (2) places of cryogenic volcanism; (3) macrocaves, minicaves, and microcaves in the icy layer connected with cryovolcanic processes; (4) the brine-filled cracks in icy crust caused by tidal forces; (5) liquid-water pools on the surface that originated from meteoritic strikes; (6) sites of hydrothermal activity on the bottom of the ocean.

4. Conclusions The environments mentioned above indicate that all conditions capable of supporting life are possible on Titan. All requirements needed for exobiology—liquid water, which exists within a long geological period; complex organic and inorganic chemistry; and energy sources for support of biological processes—are on the Saturnian moon. On Earth, life exists in all niches where water exists in liquid form for at least a portion of the year. Subglacial life may be widespread among such planetary bodies as Jovanian and Saturnian satellites and satellites of other giant planets detected in our Galaxy in the last decade [38]. Low-temperature hypersaline brines have been proposed as habitats for microbial communities on Mars [39]. The existence of a rich atmosphere is the main difference of Jupiter’s moons. This atmosphere could supply the large quantity of different organic compounds to the putative ocean. There are some possible mechanisms for extensive, intimate interaction of a liquid-water ocean with the surface of the ice crust. Titan also provides insights regarding the geological and biological evolution of early Earth during its ice-covered phase. There is a huge deficiency of C in the contemporary environment, and the missing C could be contained as biomass and dissolved Corg in the putative ocean. Possible metabolic processes, such as nitrate/nitrite reduction, sulfate reduction, and methanogenesis could be suggested for Titan. Nitrate and sulfate could be predominant forms of N and S in the ocean, and nitrate and/or sulfate reduction could have been potential sources of energy for primitive life forms. Given the possibility that organic compounds may be widespread in the ocean from synthesis within hydrothermal systems that are derived from atmospheric chemistry and delivered by comets and meteorites, these putative nitrate and sulfate reducers may have been either heterotrophic or autotrophic. Furthermore, with the presence of a substantial amount of methane, the methanogenesis, along with methanotrophs, have also been energetically favorable. Excreted products of the primary chemoautotrophic organisms could serve as a source for other types of microorganisms (heterotrophs) as has been proposed for Europa [22,26,40].

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References [1] Yung YL. An update of nitrile photochemistry on Titan. Icarus 1987; 72: 468–72. [2] Lara LM, Lellouch E, Lopez-Moreno JJ, Rodrigo R. Vertical distribution of Titan’s atmospheric neutral constituents. J. Geophys. Res. 1996; 101: 23262–83. [3] Clarke DW, Ferris JP. Chemical evolution on Titan: comparisons to the prebiotic Earth. Orig. Life Evol. Biosphere 1997; 27: 225–48. [4] Lunine JI, McKay CP. Surface-atmosphere interactions on Titan compared with those on the pre-biotic Earth. Adv. Space. Res. 1995; 15: 303–11. [5] Lunine JI, Stevenson DJ. Formation of the Galilean satellites in a gaseous nebula. Icarus 1983; 52: 14–38. [6] Zahnle K, Pollack JB, Grinspoon D, Dones L. Impact-generated atmospheres over Titan, Ganymede, and Callisto. Icarus 1992; 95: 1–23. [7] Jessberge EK, Kissel J, Rahe J. The composition of comets. In: Origin and evolution of planetary and satellite atmospheres. Tucson: University of Arizona Press; 1989. p. 167–91. [8] Whittet DCB, Schutte WA, Tielens AGGM, Boogert ACA, de Graauw T, Ehrenfreund P, Gerakines PA, Helmich FP, Prusti T, van Dishoeck EF. An ISO SWS view of interstellar ices: first results. Astron. Astrophys. 1996; 315: L357–60. [9] Griffith AC, Zahnle K. Influx of cometary volatiles to planetary moons: the atmospheres of 1000 possible Titans. J. Geophys. Res. 1995; 100: 16907–22. [10] English M, Lara LM, Lorenz RD, Ratcliff PM, Rodrigo R. Ablation and chemistry of meteoritic materials in the atmosphere of Titan. Adv. Space Res. 1996; 17: 157–60. [11] Orgel LE. The origin of life—how long did it take? Orig. Life Evol. Biosphere 1998; 28: 91–6. [12] Mancinelli RL, McKay CP. The evolution of nitrogen cycling. Orig. Life Evol. Biosphere 1988; 18: 311–25. [13] Fortes AD. Exobiological implications of a possible ammonia-water ocean inside Titan. Icarus 2000; 146: 444–52. [14] Lunine JI, Stevenson DJ. Clathrate and ammonia hydrate at high pressure: application to the origin of methane on Titan. Icarus 1987; 70: 61–77. [15] Grasset O, Sotin C. The cooling rate of a liquid shell in Titan’s interior. Icarus 1996; 123: 101–12. [16] Grasset O, Sotin C, Deschamps F. On the internal structure and dynamics of Titan. Planet. Space Sci. 2000; 48: 617–36. [17] Lunine JI. Does Titan have an ocean? a review of current understanding of Titan’s surface. Rev. Geophys. 1993; 31: 133–49. [18] Lorenz RD. Of course Ganymede and Callisto have oceans: application of a principle of maximum entropy production to icy satellite convection. [abstract]. In: Proceedings of the 32nd Lunar and Planetary Science Conference; 2001. Abstract No. 1160. [19] Spohn T, Schubert G. Oceans in the icy Galilean satellites of Jupiter? Icarus 2002; in press. [20] Zolotov MY, Shock EL. Mass balance constraints on the elemental composition of the ocean on Europa [abstract]. In: Proceedings of the 31st Lunar and Planetary Science Conference; 2000. Abstract No. 1580. [21] Ottley CJ, Davison W, Edmunds WM. Chemical catalysis of nitrate reduction by iron (II). Geochim. Cosmochim. Acta 1997; 61: 1819–28. [22] Chyba CF. Energy for microbial life on Europa. Nature 2000; 403: 381. [23] Chyba CF, Hand KP. Life without photosynthesis. Science 2001; 292: 2026–7. [24] Chyba CF, Phillips CB. Possible ecosystems and the search for life on Europa. PNAS 2001; 98: 801–4. [25] Simakov MB. Possible biogeochemical cycles on Titan. 2003. in press. [26] Gaidos EJ, Nealson KH, Kirschvink JL. Life in ice-covered oceans. Science 1999; 284: 1631–3. [27] Simakov MB. Dinitrogen as a possible biomarker for exobiology: the case of Titan. In: Lemarchand GA, Meech KJ, editors. Bioastronomy ’99: a new era in bioastronomy. Chelsea: Sheridan Books; 2000. p. 333–8. [28] Jetten MSM, Strous M, van de Pas-Schoonen KT, Schalk J, van Dongen UGJM, van de Graaf AA, Logemann S, Muyzer G, van Loosdrecht MCM, Kuenen JG. The anaerobic oxidation of ammonium. FEMS Microbiol. Rev. 1999; 22: 421–37. [29] Pizzik AJ, Sommer SE. Sedimentary iron monosulfides: kinetics and mechanism of formation. Geochim. Cosmochim. Acta 1981; 45: 687–9. [30] Stumm W, Morgan JJ. Aquatic Chemistry. New York: John and Wiley and Sons; 1981. p. 1022. [31] Lowe KL, DiChristina TJ, Roychoudhury AN, van Cappellen P. Microbiological and geochemical characterization of microbial Fe (III) reduction in salt marsh sediments. Geomicrobiol. J. 2000; 17: 163–78. [32] Lovley DR. Microbial reduction of iron, manganese, and other metals. Adv. Agron. 1995; 54: 175–231. [33] Tamegai H, Li L, Masui N, Kato C. A denitrifying bacterium from the deep sea at 11,000-m depth. Extremophiles 1997; 1: 207–11.

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[34] Hinrichs KU, Hayes JM, Sylva SP, Brewer PG, DeLong EF. Methane-consuming archaebacteria in marine sediments. Nature 1999; 398: 802–5. [35] Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke A, Amann R, Jorgensen BB, Witte U, Pfannkuche O. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 2000; 407: 623–6. [36] Michaelis W, Seifert R, Nauhaus K, Treude T, Thiel V, Blumenberg M, Knittel K, Gieseke A, Peterknecht K, Pape T, Boetius A, Amann R, Barker B, Widdel F, Peckmann J, Pimenov NV, Gulin MB. Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane. Science 2002; 297: 1013–5. [37] Simakov MB. The possible sites for exobiological activity on Titan. In: Proceedings of the First European Workshop on Exo/Astrobiology. Frascati, Italy 21–23, May 2001. p. 211–4. [38] Perryman MAC. Extra-solar planets. Rep. Progr. Phys. 2000; 63: 1209–72. [39] Wynn-Williams DD, Cabrol NA, Grin EA, Haberle RM, Stoker CR. Brines in seepage channels as eluants for subsurface relict biomolecules on Mars? Astrobiology 2001; 1: 165–84. [40] Boston PJ, Ivanov MV, McKay CP. On the possibility of chemosynthetic ecosystems in subsurface on Mars. Icarus 1992; 95: 300–8.

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The Role of Living and Nonliving Organic Matter in Volkonskoite Formation Y.S. SIMAKOVA Institute of Geology RAS, Pervomaiskaya St., 54, 167982, Syktyvkar, Russia Tel. 7 8212 446534; Fax: 78212 245346; e-mail: [email protected] Abstract. New data on the composition and genesis of volkonskoite, based on mineralogical investigation of the mineral are presented. Scanned electron microscopy (SEM) investigations of volkonskoites reveal an undoubted role of bacterial activity in volkonskoite formation, i.e.: in the chromium (Cr) concentration and fixation in the smectite structure.

Introduction The processes of the interaction between minerals and organic matter are of great scientific and practical interest because they often result in the formation of mineral deposits of unusual types in sedimentary rocks. The volkonskoite mineralization in the Upper Permian sandstones in West Ural is one of them. Volkonskoite is a unique mineral from the smectite group, containing dominant Cr in the octahedral position. This mineral is formed on different organic remains buried in productive sandstones from West Ural (Perm and Kirov region). Volkonskoite occurs in the form of veinlets, and it often forms complete pseudomorphs of even large tree trunks (volkonskoite tree) and sometimes cements or replaces clastogenic rock grains in sandstones. The presence of Cr, vanadium (V), and nickel (Ni) in the primary terrigenous material is related to the formation of the sequence due to the destruction of the greenstone zone rocks and the ancient weathering crusts of Urals, which include large deposits of magmatogenic chromites in this area [1]. 1. Materials and Methods In 1994, specimens of volkonskoite and volkonskoite-bearing rocks were collected by the author from six occurrences in West Ural (Perm and Kirov regions). All volkonskoite samples were examined by different techniques: chemical analysis, SEM and microprobe analysis, x-ray diffraction, electron paramagnetic resonance (EPR), infrared spectroscopy (IRS), and chromato-mass spectrometry.

2. Results and Discussion Chemical analysis of volkonskoite shows great variations in Cr content (15–30 wt.%), and in volkonskoite-bearing rocks, Cr accumulates in the clayey cement of sandstones

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Figure 1. SEM micrographs of volkonskoite: (a) microglobular, (b) acicular, (c) curved-plated, and (d) loopshaped (crystallized gel texture).

(Cr2O3~2 wt.%). The samples of volkonskoite with high-Cr contents (~30 wt.%) have been found in the West Ural rocks for the first time. Such a high concentration of Cr in the mineral cannot be caused by the Cr sorption on clays. It can be propose that the reason for volkonskoite formation is the interaction of Cr solutions with microorganisms and plant organic matter. Despite the fact that the role of organic matter as a Cr concentrator in volkonskoite formation is evident, the gas chromatographic and EPR investigations show that initial organic matter in volkonskoites and enclosing rocks is absent. DNA extraction of volkonskoite samples also gives no results. However, SEM observations permit us to detect some biosignatures in the mineral. Unsubstituted by volkonskoite relics of silicified wood from the volkonskoite tree and veinlets keep the inner structure of the replaced tree. The mineral has a fine fibrous texture with fragments of ligneous sells. In the case of a complete volkonskoite substitution, the primary structure of wood is sometimes fully lost. In relics of silicified wood, unsubstituted by volkonskoite, Cr accumulates first on clayey matter that has been formed on cell membranes, boundaries of quartz grains, small cracks, and other places where organic matter can remain and microorganisms can grow. SEM investigations of volkonskoites show the presence of different textures in this mineral—globular, acicular, curved-plated, and loop-shaped (Fig. 1). All of these textures are widespread among smectites and typical for the products of gel crystallization. Massive microglobular texture occurs in volkonskoite more frequently than any other type of texture. Microglobules consist of curved-plated particles with different orientations; particle size is about 200 to 600 nm. Also, the unique volkonskoite vermicular texture (Fig. 2) was found. The islets of mineral with vermicular texture are irregularly spaced among massive volkonskoite and have the same chemical composition. Separate volkonskoite particles in this particular type of texture have a curved shape, typical for some species of bacteria, and can be interpreted as colonies of fossilized bacterial cells with a particle size of about

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Figure 2. SEM micrographs of bacterial-like particles in volkonskoite.

200 to 400 nm. Similar bacterial cells are often observed in the mineral surface and in the inner parts of minerals [2,3]. The morphology of the vermicular particles is analogous to the morphology of Crreduced bacteria that were described in microbiological articles [4,5]. Atomic force microscope studies provided the information on the surface topography of volkonskoite samples. The mineral surface consists of globular particles with a size of about 200 to 350 nm, the morphology and size range of the globules could also mean that they were crystallized from the fossilized bacterial cells. Bacterial activity could promote the decay of the buried organic remains and the reduction of Cr6+ to its insoluble state during volkonskoite formation. So, the reduction and fixation of Cr in clay minerals may be provided by microorganisms or by ferrous iron (Fe), which is microbiologically reduced from ferric Fe, and vermicular particles of volkonskoite are the signs of previous bacterial activity. A broad variety of bacteria able to reduce chromate has been found [6]. Observation of bacterial structures in volkonskoite samples is evidence of an undoubted role that is played by living organic matter in volkonskoite formation. Volkonskoite with microglobular texture is the result of the crystallization of silicon- (Si-) Cr gel supplied by bacterial activity. The inner structure of volkonskoite and silicified wood fragments are often marked by finely disseminated inclusions of Fe hydroxides, so the presence of ferric and ferrous Fe can promote the concentration and fixation of Cr in clayey matter. Inner structure of the inclusions (d~10 to 15 μm) indicates their organic origin (Fig. 3). Such inclusions have a rounded shape with a cellular interior, where Cr and Fe have an inverse distribution: Cr concentrated in the interior of the inclusion and Fe, preferentially in the border. The inclusions of Fe hydroxides preserve better in silicified wood relics than in volkonskoite samples, where they are altered but still display their organic origin. The accumulation of Cr in silicified wood takes place first in the Fe-inclusions (Fig. 4). This supposition about biochemogenic volkonskoite formation is also supported by the probable biogenic origin of Fe-inclusions in this mineral, where Fe2+ promoted the Cr6+ to Cr3+ reduction as an electron acceptor, simultaneously fixing Cr in the environment. Samples of the high-Cr volkonskoites (Cr2O3 ~30 wt.%) appear to be a mixture of two (or more) phases—dioctahedral smectite and interstratified smectite-vermiculite—where different phases are thought to be connected with the different parts of the replaced wood

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Figure 3. SEM micrographs of Fe-inclusions in the cilicified wood relic from volkonskoite tree—bright: Feinclusions and dark: quartz.

Figure 4. EDS maps of Fe-inclusion from Fig. 3, b: distribution of Cr, Fe, Si and V.

structure. Cromium6+ is known to be easily reduced to Cr3+ by contact with wood, forming stable chemical compounds of the hydrated Cr-oxide type [7]. So, unusually high Cr content in some volkonskoite samples can be caused by direct interaction of Cr solution with the plant organic matter. The accumulations of lens-shaped particles with a high content of cerium (Ce) and manganese (Mn) from the enclosing sandstone at the boundary of the volkonskoite tree (Fig. 5) can also be signs of bacterial activity and the result of biogenic accumulation of heavy metals at the volkonskoite-bearing rocks.

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Figure 5. SEM micrographs of Ce-Mn lens-shaped particles from the boundary of volkonskoite tree with sandstone.

3. Conclusions An important role of organic matter (living and dead) in volkonskoite formation has been confirmed by microscopic investigations of the mineral, silicified wood fragments, and enclosing rocks. The islets (or relics) of volkonskoite with vermicular texture among the massive mineral texture can be interpreted as colonies of fossilized bacterial cells and particles of massive volkonskoite as the result of fossilized material crystallization. Unusually high Cr concentration (up to 30% Cr2O3) in high-Cr volkonskoite is stipulated for the interaction of Cr solutions and initial organic matter of buried plant remains. This type of interaction leads to the formation of mineral with abundant Cr that is fixed in the interlayered positions of smectite structure. The inclusions of Fe hydroxides finely disseminated in volkonskoite also have an organic origin, so the presence of biogenic ferric and ferrum iron can promote the concentration and fixation of Cr in the mineral. The volkonskoite can be considered to be the result of complicated interaction of microbially transformed organic matter with Si-Cr gel, biogenic Fe, and perhaps, Cr-reduced bacteria. It is expedient to continue such studies using modern methods of investigation for understanding the processes of heavy metal mineralization in sedimentary rocks.

Acknowledgements The author is grateful to V.N. Filippov for providing the SEM data used in this study.

References [1] Kossovskaya AG, Gomon’kov AV, Gor’kova NV, Shchepetova EV. New data on the composition and genesis of volkonskoite. Lithol. & Miner. Resources 1996; 31(2): 129–38. [2] Geptner AR, Ivanovskaya TA. Biochemogenic genesis of the glauconite-nontronite series minerals in present-day sediments of the Pacific ocean. Lithol. & Miner. Resources 1998; 6: 563–80.

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[3] Little BJ, Wagner PA, Levandovski Z. Spatial relationship between bacteria and mineral surfaces. In: Banfield JF, Nealson KH, editors. Geomicrobiology: Interaction between microbes and minerals, Washington, D.C.: Reviews in mineralogy 35; 1987. p. 123–59. [4] Lebedeva YeV, Lyalikova NN. Reduction of crokoite by the culture of Pseudomonas Chromatophila Sp. Nov. Microbiol. 1979; 48(3): 517–22. [5] Romanenko VI, Koren’kov VN. Pure bacterial culture used chromates and bichromates as hydrogenium acceptor for its development in anaerobic conditions, Microbiol. 1977; 46(3): 414–9. [6] Nies DH. Microbial heavy-metal resistance. Appl. Microbiol. Biotechnol. 1999; 51: 730–50. [7] Jorge FS, Santos TM, de Jesus JP, Banks WB. Reactions between Cr(VI) and wood and its model compounds, Wood Sci. Technol. 1999; 33: 501–17.

Perspectives in Astrobiology R.B. Hoover et al. (Eds.) IOS Press, 2005 © 2005 IOS Press. All rights reserved.

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Astrobiotechnology: Alternative Concepts for Astrobiology Solar System Exploration Jan TOPORSKI and Andrew STEELE Carnegie Institution of Washington, Geophysical Laboratory, 5251 Broad Branch Road N.W., Washington D.C., 20015-1305, USA Abstract. A key issue in astrobiology research is and has been to understand the origin, evolution, and distribution of life on Earth and in the solar system. Consequently, crucial to this endeavor is the identification of means to unambiguously detect evidence of life. Efforts to identify traces of life in extraterrestrial materials or even remotely on the surface of Mars have resulted in ambiguous, non-conclusive information. As a result it has recently been proposed to pursue alternative technologies to help answer the challenge presented by the search for life elsewhere in the solar system. Here, an integration of approaches and technologies, developed and applied mainly in molecular biology and biotechnology with astrobiology is introduced. The overall concept behind this approach is to employ molecular biology tools and biotechnology to detect specific astrobiologically and geobiologically relevant target molecules. This is based around the high sensitivity, specificity, and affinity of proteins (antibodies) or DNA/RNA aptamers to a series of target molecules that define extinct and extant terrestrial life or prebiotic components. Advanced DNA and protein chip technology can be utilized to allow thousands of multiple tests in a single analytical step. Microarray technology can be combined with microfluidics to ultimately achieve high sensitivity and specificity in a lightweight automated device designed for solar system exploration.

Introduction As a general trend in modern science, it has emerged that individual areas of research may provide corroborative information to a common question, leading to the realization of the important role that interdisciplinary research can play in comprehensively answering such questions. Two major fields within the natural sciences for which this has come particularly true are the biosciences and geosciences, evidently endorsed by the emergence of new disciplines, such as geobiology, geomicrobiology, and astrobiology. Lately, these fields have become more exposed in the public domain due to eminent scientific controversies concerning the earliest evidence of life on Earth [1–5] and the continuing discussions over possible evidence of biogenic activities in Martian meteorite ALH84001 [6–9]. The common denominator in these debates is the underlying difficulty or inability to conclusively demonstrate the biogenicity of the respective evidence, which—in either of the above cases— would be evidence of fossil microbial life. A step closer to a possible solution is the combination of morphological with chemical information. Carbon (C) isotopes have been successfully correlated with individual Proterozoic microfossils [10] and Fourier transformRaman spectra were obtained on supposed Early Archaean microfossils [11], although this evidence is far from being conclusive [4]. Notably, Toporski et al. [12] demonstrated the possibility of correlating more comprehensive molecular information with fossil bacterial

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biofilms using time of flight-secondary ion mass spectroscopy, a technique that has been shown to be capable of detecting unambiguous biomarkers in complex organic mixtures [13,14]. However, a great deal of further systematic experimentation must be undertaken in order to answer those questions conclusively. Crucial aspects in solar system exploration seeking to understand the distribution of life in our solar system and ultimately the universe (as defined in the Astrobiology Road Map Goals 2, 3, 4, 5, and 7 [15]) are determined by detection sensitivity and the technical requirements of the respective instrumentation as well as the specifications and robustness of the technology applied. Although promising, analytical instruments applied in the studies described above can only be considered for Earth-based investigations due to their size, weight, energy requirements, and complexity, which with the currently available space flight technology would render remote and robotic operation virtually impossible. Intimately connected with all goals of the Astrobiology Road Map [15], indicated above, are issues addressed in Goal 7, to determine how to recognize signatures of life on other worlds and on early Earth. The discussions indicated earlier hint at the difficulties associated with this endeavor. Taking the issue even further, research on the Martian meteorite, ALH84001 [16], has shown that techniques purported to detect life signals with great sensitivity were shown to have failed to detect terrestrial contaminating organisms within this meteorite. Not surprisingly many other meteorites have been shown to be contaminated, some from the external fusion crust through to the core [17,18]. As a consequence of this scientific dilemma, there seems to be the need in astrobiological research to consider alternative concepts in solar system exploration. Therefore, new strategies are proposed for solar system exploration involving biotechnology and specific recognition molecules—target molecule interactions to detect the possible presence of bacterial biomarkers (both extinct and extant) in rocks [19]. This approach explores the use of antibodies raised to specific viable and fossil marker molecules to search for the possible presence of molecular biomarkers in rocks. Antibodies have previously been successfully raised to individual proteins within bacteria or whole bacterial species; individual amino acids; organic pollutants, e.g.: polycyclic aromatic hydrocarbons; DNA; RNA; and important prokaryotic proteins, extracellular polymers, and enzymes. Immunological techniques have also been used to assay for traces of extinct life targeting compounds including DNA, proteinaceous matter, hopanes, hemoglobin, collagen, and keratin [20–26]. It is therefore conceivable that this approach may be tailored specifically to scientific needs to detect traces of bacterial activities in rocks, regardless of whether extinct or extant or of whether terrestrial or extraterrestrial. This technique can also be expanded to use a number of probes (not exclusively antibodies) for detection of suitable target molecules including oligonucleotides, DNA, and enzymes. If life existed—or even exists—elsewhere in the solar system or universe and, indeed, followed principles employed by life on Earth, then one must assume that it is most likely to be represented by single-celled prokaryotic microorganisms. Evidence of extinct life on Mars or Europa may still be present in the form of potentially detectable molecular biomarkers in the Martian surface regolith, in subsurface rock formations, or in Europa’s ice layers. A brief summary of relevant bacterial biomarker molecules can be found in the work by Toporski and Steele [27].

1. A Biotechnological Approach to the Detection of Life The growth of biotechnology in the last 20 yr has been staggering, and the sheer number of new techniques and procedures can be disorienting. With the birth of astrobiology, a natural interface between biology and therefore biotechnology, space, and geological sciences has

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been formed. Here, the goal is to bring together a cross section of the latest research and development in biotechnology instrumentation and, particularly, in biosensors that are relevant in a solar system exploration context. A list of biotechnology techniques, which are applicable to miniaturization and integration into an astrobiology science platform is given in the following: • • • • • • • • • • • •

Use of antibodies. Fluorescent detection strategies. Protein and DNA chip technology. Surface plasmon resonance and its relation to other techniques. Microelectronic machining (where applicable to biological systems). Nanotechnology (where applicable to biological systems). Lab-on-a-chip technology (including polymerase chain reaction (PCR)). Mass spectrometry (matrix assisted laser desorption ionization-time of flight mass spectrometry). Fluid handling and extraction technologies (micro fluidics). Chemical force microscopy (CFM). Raman spectroscopy. Nanotechnology (molecular motors).

The development and integration of these techniques would fulfill a unique purpose in exploration terms and the detection and, more importantly, the potential characterization of life in various terrestrial environments and on other solar system bodies. Why use biotechnology? The techniques used thus far for solar system exploration have been ambiguous or failed completely to detect life. In the case of the debate on relic biogenic activity in the Martian meteorite, ALH84001, many traditional techniques, such as amino acid analysis, C-isotope analysis, and gas chromatography-mass spectrometry (GCMS), all concluded that no life was contained within the meteorite [6,7,28,29]. However, some of the (if not the entire) meteorite was colonized by terrestrial microbiota [16]. Whether through reasons of sample selection, choice of technique, or detection sensitivity, this organism was not found by the techniques traditionally associated with life detection in the solar system and the techniques that are being developed for flight instrumentation. Another example is the ambiguity associated with the Viking Lander results [30]. Recent reevaluations of these experiments have revealed that the sensitivity of the GC-MS was simply inadequate for the task and would have missed the organic material produced by approximately 107 bacteria per gram of Martian regolith [31]. This ambiguity (through inadequate instrumental analytical tolerances) must be prevented from re-occurring in future exploration efforts. Within biology, if a patient has an infection, there is a food spoilage problem, or a novel organism is sought to answer specific biology (biotechnology) questions, the techniques of choice are not isotopic or amino acid analysis, Raman spectroscopy, or even GC-MS (techniques currently being adapted for space flight in the search for evidence of extraterrestrial life). A wealth of microbiological, molecular, and genetic techniques, which are now being refined as biotechnology approaches what is widely regarded as its golden age, have been developed. The human genome has been sequenced, as have the genomes of a host of plants, animals, and bacteria. Miniaturization and nanotechnology have been integrated with biotechnology in exciting new fields of research towards the goal of lab-on-a-chip instruments [32,33]. To put it simply, these techniques have been developed to answer, on Earth, the questions that need to be addressed in the rest of the solar system: Is there or was there (ever) microbial life present? What are its characteristics? How can it be detected in small abundances? What effects does it have on the environment in which it resides, and vice versa? Whether it is a novel microbe in a black smoker or an unknown infection in the

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human body, the task, goals, methodology, and philosophy are the same. To the question: Why use biotechnology? The answer is: Because it was developed for this task and need only be modified to be applied to astrobiology and to solar system exploration. There are several categories of molecules of astrobiological interest that must be detected and then distinguished from each other. These categories include: • • • •

•

•

Prebiotic molecules—amino acids, individual nucleotides, polycyclic aromatic hydrocarbons, and alkanes. Terrestrial contaminating organisms—whole cells, cell components (LPS, DNA, and proteins). Terrestrial contaminating organics—rocket exhaust, lubricants, plastics, biomolecules. Terrestrial-like organisms—transferred from Earth to an extraterrestrial body or have evolved on the extraterrestrial body in a similar manner to which life evolved on Earth. Examples of target molecules could include individual genes, membrane components, and enzymes. Non-terrestrial-like organisms—evolved on similar biochemistry but has selected different molecules to carry out information storage, information transfer, compartmentalization, and enzymatic activity; an example would be the use of novel amino acids or nucleotides (combinatorial chemistry; see below). Fossil biomarkers—detection of known terrestrial fossil biomarkers such as hopanes, archaeal lipids and steranes, or the detection of the diagenetic remains of an alien biochemistry.

Over the last decade, the drive to miniaturize common laboratory techniques has produced systems that are relevant for astrobiological research and solar system exploration. A selection of which are outlined in Sections 1.1 through 1.3. 1.1. Microfluidics Based on technology transported from the silicon conducting industry and fuelled by clinical considerations, there are currently microfluidics based systems, which can perform a number of linked tasks using micro-liter (or even less) volumes of analytes and reagents. These include capillary electrophoresis for DNA, RNA, and protein separation and analysis; flow cytometry; PCR; mass spectrometry; microarray inoculation; enzyme-linked immunoabsorbent assay; and sample separation, processing, i.e.: enzyme reaction, and concentration of target analytes. Several microfluidic designs also exist for cell culturing chambers that screen hundreds of different growth media for growth of a target organism or community [34]. The growth and scope of these systems can be found elegantly reviewed by Reyes et al. [32] and Auroux et al. [33]. 1.2. Microarrays Originally designed for high-throughput data mining of genomes, these arrays can fit up to several million separate tests per glass slide [35,36]. This technology is growing at an unprecedented rate and will revolutionize environmental microbiology (including issues relevant in astrobiology and geobiology). Although these tests comprise mostly DNA- and protein-based tests, their use can be diversified to any test using any reagents that produce a color change (either chromophore or fluorophore) during the detection of a primary molecule. The technology is commercially available and being utilized to produce miniaturized, highly specific test kits for a range of organic compounds linked to life processes and, indeed, has been highlighted for further development by a number of agencies [37]. These

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test kits could be tailored for use in all of the points above. A further interesting possibility for the detection of extraterrestrial life arises if one considers combining combinatorial chemistry and microarray technology. It would then be possible to produce millions of random probes per glass slide that contain all the possible combinations of purine and pyrimidines bases that can combine into an information storing system complex enough to code for an organism. This, then, reduces the assumptions needed for the detection of an extraterrestrial organism from DNA-based life to that of nucleic acid-based life. These techniques may be further refined for use in experiments on the formation of life on Earth by screening large numbers of prebiotic reactions printed onto glass slides and/or mineral interfaces. 1.3. Probe Design Many of the techniques used to find life are centered on probe technology. The essence of this technique is the use of a detector molecule that is linked to a substrate or reporter molecule. Interaction of the target molecule and the probe is then detected in some manner. Examples of currently used probes follow: •

•

•

Nucleic acids—short strands of DNA and RNA that can recognize and specifically bind to both complimentary strands of DNA and cell surface proteins and are commonly used linked to a reporter molecule, such as fluorescent markers, in such techniques as fluorescent in situ hybridization, and flow cytometry [38]. Small RNA or DNA molecules, also referred to as aptamers, can be used in the detection of not only other nucleic acids but small organic molecules [39–41]. Antibodies—both monoclonal and polyclonal antibodies exist for a range of targets of astrobiological interest, including prebiotic chemicals, whole cells, DNA, cell wall components (including species specific lipopoly-saccharides), proteins, porphyrins, petroleum, and fossil biomarkers, such as melanoidins and hopanes. Enzymes—enzymes as recognition molecules are applied in the limulus amebocyte lysate (LAL) assays [42].

The problem then remains to detect the reaction between the probe and the target molecule. A short list of common detection methodologies is as follows—for an in-depth review of these techniques, see Nakamura et al. [43]: • • • • • • • • •

Color change (visible light or fluorescence which is then detected by microscopy). Gold labeling (detected using electron microscopy). Measurement of change in electrical conductivity or potential. Surface plasmon resonance. Gravitometric techniques. Optical interferometry. CFM. Mass spectrometry. Liquid chromatography.

2. Integration of Biotechnology into Astrobiology The ultimate goal is to achieve the integration of biotechnology into astrobiological research, which requires a capacious approach as outlined in Fig. 1. Geoscience and astrobiology groundwork involves research that characterizes and seeks to understand the processes involved in the preservation of the evidence for life in the fossil record.

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Figure 1. Schematic illustration of research and development steps involved in the integration of biotechnology into astrobiology for solar system exploration.

Concomitant with this, the identification of target molecules, i.e.: biomarkers, will continue, and this knowledge is then immediately relevant for the molecular biology and biotechnology aspects of this concept. Suitable probes will have to be identified and be produced, which subsequently will be applied in microchip design. Probes and microchips will then be tested in constrained experiments and complex environmental scenarios. Clearly, all these steps are linked, thus communication between the various experimental and developmental levels and during testing phases is imperative to develop the approach to a degree that it may be integrated into an analytical science platform for solar system exploration. 2.1. Modular Assays for Solar System Exploration The modular assays for solar system exploration (MASSE) system [44] seeks to use the above outlined technologies and approaches to search for life in the solar system. The instrument will use microchip-based microfluidic systems to accept, extract, concentrate, filter, buffer, and process molecules of interest from a sample handling chamber. Several commercial instruments are being developed that achieve the same goal [34]. The system will then separate and deliver these to a range of reaction areas including enzyme assays, such as the LAL assay, antibody and/or aptamer/DNA microarrays, as well as to flow cytometry chambers. Further techniques that are currently being investigated for integration into a modular instrument design include PCR, capillary electrophoresis systems, and mass spectrometry. Currently we are examining both fluorescence and electrochemical detection methods with a prototype design based on laser fluorescence detection. The MASSE system is currently further considered to be integrated in a science platform called Mars Exobiology Multi-User Facility [45], which is part of the European Space Agency’s (ESA’s)

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most recent Mars exploration effort. Initially funded by NASA and recommended for further development by ESA, this instrument has recently fulfilled its proof of concept goals. Further information of the proposed instrument can be found at the MASSE Web site [46].

3. Summary The emerging field of astrobiology, as well as disciplines such as geobiology and geomicrobiology, can benefit hugely by embracing the latest in biotechnology for studies on Earth and for robotic and human space exploration. To achieve this, particularly with respect to astrobiology-related research, before NASA’s next bid to look for biomarkers on the Mars missions of 2009 and beyond and ESA’s Mars astrobiology exploration program AURORA (including the anticipated ExoMars flagship mission containing the PASTEUR analytical platform) [45,46], a synthesis of geobiologists and astrobiologists with molecular biologists and biotechnologists with space flight engineers from both commercial and academic communities will be required. That is why the formation of a NASA Astrobiology Institute focus group called Astrobiotechnology is being proposed to encourage this necessary interface and enable a forum for discussion of common research ground, probe design, the nature of extraterrestrial life and its detection, and to identify common funding routes (see the Astrobiotechnology Focus Group link at the MASSE Web site [47] for further information). It is only by promoting this interface that the answer to the question of life in the solar system can be unambiguously answered within a foreseeable timeframe.

Acknowledgements Thanks go to Jake Maule, David S. McKay, and Kennda Lynch (NASA Johnson Space Center, Houston, Texas, United States); Victor Parro Garcia, Carlos Briones, and Juan Pérez-Mercader (Centro de Astrobiologia, Madrid, Spain); Mary Schweitzer and Recep Avci (Montana State University, Bozeman, Montana, United States); Frances Westall (Center de Biophysique Moleculairee, CNRS, Orleans, France); Marilyn Fogel, Wesley Huntress, Bob Hazen, and George Cody (Carnegie Institution of Washington, Geophysical Laboratory, Washington DC, United States); Norm Wainwright (Marine Biology Laboratory, Woods Hole, United States); Judson Hedgecock and Rachel Robertson (Oceaneering Space Systems, Houston, Texas, United States); Seth Pincus (New Orleans Children’s Hospital, New Orleans, United States); and Huw Rowlands (Blue Sky Project Management, Portsmouth, United Kingdom).

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[7] Jull AJT, Courtney C, Jeffrey DA, Beck JW. Isotopic evidence for a terrestrial source of organic compounds found in Martian meteorites Allan Hills 84001 and Elephant Moraine 79001. Science 1998; 279: 366–9. [8] Golden DC, Ming DW, Schwandt CS, Lauer HV, Socki R, Morris R, Lofgren GE, McKay GA. Inorganic formation of zoned Fe-Mg-Ca carbonate globules with magnetite and sulphide rims similar to those in Martian meteorite ALH84001 [abstract]. In: Proceedings of the 31st Annual Lunar and Planetary Science Conference; 2000; Houston (TX) Lunar and Planetary Institution; 2000, Abstract No. 1799. [9] Thomas-Keprta KL, Clemett SJ, Bazylinski DA, Kirschvink JL, McKay DS, Wentworth SJ, Vali H, Gibson EK Jr, McKay MF, Romanek CS. Special feature: truncated hexa-octahedral magnetite crystals in ALH84001: Presumptive biosignatures, Proc. Natl. Acad. Sci. 2001; 98: 2164–9. [10] House CH, Schopf JW, McKeegan KD, Coath CD, Harrison TM, Stetter KO. Carbon isotopic composition of individual Precambrian microfossils. Geology 2000; 28: 707–10. [11] Schopf JW, Kudryavtsev AB, Agresti DG, Wdowiak TJ, Czaja AD. Laser-Raman imagery of Earth’s earliest fossils. Nature 2002; 416: 73–6. [12] Toporski J, Steele A, Westall F, Avci R, Martill M, McKay DS. Morphological and spectral investigation of exceptionally well preserved bacterial biofilms from the Oligocene Enspel formation, Germany. Geochim. Cosmochim. Acta 2002; 66: 1773–91. [13] Steele A, Toporski JKW, Avci R, Guidry SA, McKay DS. Time of Flight – Secondary Ion Mass Spectrometry (ToF-SIMS) of a number of bacterial hopanoids. Organic Geochem. 2001; 32: 905–11. [14] Toporski J. The preservation and detection of morphological and molecular bacterial biomarkers and their implications for astrobiological research. [Ph.D. Thesis]. Portsmouth, UK: University of Portsmouth; 2001. [15] http://astrobiology.arc.nasa.gov/roadmap. [16] Steele A, Goddard DT, Stapleton D, Toporski JKW, Peters V, Bassinger V, Sharples G, Wynn-Williams DD, McKay DS. Imaging of an unknown organism on the Martian meteorite ALH84001. Met. Plan. Sci. 2000; 35: 237–41. [17] Toporski JKW, Steele A, Westall F, Griffin C, Whitby C, Avci R, McKay DS. Electron microscopy studies, surface analysis and microbial culturing studies on a depth profile through Martian meteorite NAKHLA [abstract]. In: Proceedings of the 31st Annual Lunar and Planetary Science Conference; 2000; Houston (TX); Lunar and Planetary Institution; 2000, Abstract No. 1636. [18] Gillet Ph, Barrat JA, Heulin Th, Achouak W, Lesourd M, Guyot F, Benzerara K. Bacteria in the Tatahouine meteorite: nanometric-scale life in rocks. Earth Plan. Sci. Let. 2000; 175: 161–7. [19] Steele A, Toporski J. Astrobiotechnology. Second European exo- and astrobiology workshop. Graz, Austria; 2002 September 16–19; Noordwijk, the Netherlands: ESA Publication Division: ESA SP–518 2003; in press. [20] De Jong EW, Westbroek P, Westbroek JF, Bruning JW. Precervation of antigenic properties in macromolecules over 70 million years old. Nature 1974; 252: 63–4. [21] Westbroek P, van der Meide PH, van der Wey-Kloppers JS, van der Sluis RJ, De Leeuw JW, De Jong EW. Fossil macromolecules from cephalopod shells: characterization, immunological response and diagenesis. Paleobiology 1979; 5: 151–67. [22] Muyzer G, Westbroek P, DeVrind JPM, Tanke J, Vriheid T, De Jong EW, Bruning JW, Wehmiller JF. Immunology and organic geochemistry. Org. Geochem. 1984; 6: 847–55. [23] Child AM, Pollard AM. A review of the applications of immunochemistry to archaeological bone. J. Arch. Sci. 1992; 19: 39–470. [24] Nerlich AG, Parsche F, Kirsch T, Wiest I, von der Mark K. Immunohistochemical detection of interstitial collagens in bone and cartilage tissue remnants from an infant Peruvian mummy. Am. J. Phys. Anthro. 1993; 91: 279–85. [25] Schweitzer MH, Horner JR. Intravascular microstructures in trabecular bone tissues of Tyrannosaurus Rex. Annales de Paleontologie 1999; 85: 179–92. [26] Maule J, McKay DS, Toporski J, Lynch K, Lindsay J, Hedgecock J, Wainwright N, Steele A. Using antibodies to detect unambiguous biomarkers. [abstract]. Abstract of the NAI all-hands meeting; 2002 February 10–12 Tempe (AZ): Arizona State University; 2003. [27] Toporski J, Steele A. The relevance of bacterial biomarkers in astrobiological research. Second European exo- and astrobiology workshop. Graz, Austria; 2002 September 16–19; Noordwijk, the Netherlands: ESA Publication Division: ESA SP–518 2003; in press. [28] Bada JL, Glavin DP, McDonald GD, Becker L. A search for endogenous amino acids in Martian meteorite ALH84001. Science 1998; 279: 362–5. [29] Clemett SJ, Dulay MT, Gilette JS, Chillier XDF, Mahajan TB, Zare RN. Evidence for the extraterrestrial origin of polycyclic aromatic hydrocarbons (PAHs) in the Martian meteorite ALH 84001. Faraday Discussions (Royal Soc. Chem.) 1998; 109: 417–36. [30] Mancinelli RL. Prospects for the evolution of life on Mars, Viking 20 years later. Adv. Space Res. 1998; 22: 471–7.

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[31] Glavin DP, Schubert M, Botta O, Kminek G, Bada JL. Detecting pyrolysis products from bacteria on Mars. Earth Plan. Sci. Let. 2001; 185: 1–5. [32] Reyes DR, Iossifidis D, Auroux P-A, Manz A. Micro Total Analysis Systems. 1. introduction theory and technology. Anal. Chem. 2002; 74: 2623–36. [33] Auroux P-A, Iossifidis D, Reyes DR, Manz A. Micro total analysis systems. 2. analytical standard operations and applications. Anal. Chem. 2002; 74: 2637–52. [34] Fitzgerald DA. Making every nanolitre count. The Scientist 2001; 15: 26. [35] Hoheisel JD. Oligomer chip technology. Trends in Biotechnology 1997; 15: 465–9. [36] Schena M, editor. Microarray biochip technology. Natick (MA): Eaton Publishing; 2000. 298 p. [37] Gibson G. Microarrays in ecology and evolution: a preview. Molecular Ecology 2002; 11: 17–24. [38] Gerhardt P, Murray RGE, Woods WA, Krieg NR, editors. Methods for general and molecular microbiology. Washington D.C: American Society for Microbiology; 2002. General ref. [39] Patel DJ, Suri AK, Jinang L, Fan P, Kumar RA, Nonin S. Structure, recognition and adaptive binding in RNA. J. Mol. Biol. 1997; 272: 645–664. [40] Hamaguchi N, Ellington A, Stanton M. Aptamer beacons for the direct detection of proteins. Anal. Biochem. 2001; 294: 126–31. [41] Meli M, Vergne J, Decout J-L, Maurel M-C. Adenine-aptamer complexes. J. Biol. Chem. 2002; 277: 2104–11. [42] Wainwright NR, Child A. Use of amplified microbial detection assays in life detection and planetary protection studies. [abstract]. Workshop on Mars 2001. 1999 October 2–4; Houston (TX): LPI. Abstract No. 2554. [43] Nakamura RM, Kasakara Y, Rechnitz GA, editors. Immunochemical assays and biosensor technology for the 1990’s. Washington D.C.: American Society for Microbiology; 1992. 355 p. [44] Sims MR, Pullan D, Pillinger CT, Wright IP. An evaluation of in situ analysis and sample return in the exploration of Mars. Plan. Space Sci. 2002; 50: 657–68. [45] Schulte W, Hilchenbach M, Richter L. The Mars exobiology Multi-User facility PASTEUR. Second European exo- and astrobiology workshop. Graz, Austria; 2002 September 16–19; Noordwijk, the Netherlands: ESA Publication Division: ESA SP–518 2003; in press. [46] Vago JL, Santovincenzo A, Gardini B. ESA’s mission to search for signs of life on Mars: ExoMars and the PASTEUR scientific payload. [abstract]. Abstracts of the second European exo- and astrobiology workshop. 2002 September 16–19; Graz, Austria. [47] http://www.masse.co.uk/page_8_astrobiologyform.htm.

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The Study of Remains of Microorganisms in Ancient Earth Sedimentary Rocks for Astrobiology Galina T. USHATINSKAYA, Elena A. ZHEGALLO and Emil L. SHKOLNIK Paleontological Institute RAS, Profsoyuznaya 123, Moscow, 117997, Russia Abstract. Ancient phosphorites are one of the best model objects for studying fossilized microorganisms, their morphology and sizes, types of preservation, conditions of burial, and products of life activity. These studies help understanding and interpreting biomorphic structures of the astromaterials.

Introduction For studying, understanding, and interpreting biomorphic structures of astromaterials, it is necessary to recognize and understand the biomorphic structures of Earth rocks. Their morphology, sizes, types of preservation, burial conditions, and products of habitability, which are reflected in lithological and geochemical features of enclosing rocks should be known [1,2]. It has been concluded from long scanning electron microscopy (SEM) studies of many sedimentary rocks that they could almost always, when microorganisms were present in basins, be well-preserved as fossils. The type of their preservation depends on the rock composition and the types of replacing minerals. Microorganisms are best preserved in cherts, phosphorites, carbon-rich rocks, and bauxites; preservation in carbonates is much worse. Furthermore, the study of the mentioned rocks indicates that microbiota are required for the formation of sedimentary rocks (with the exception of conglomerates and gritstones) in ancient epicontinental basins. Owing to the very great (within hours) speed of bacteria fossilization, the preservation of fossil bacteria in a number of cases is so fine (they have no time for decomposition) that they are comparable with recent microorganisms [3–5]. One of the best model objects for studying fossilized microorganisms is ancient phosphorites. The remains of microorganisms and products of their life activity are known in phosphorite structures from Early Cambrian to Tertiary ages. Lower Cambrian (Tommotian) phosphorites from Northern Mongolia (Khubsugul phosphorite basin) have long been considered as a classic example of ancient chemogenic phosphatic accumulation [6,7]. Research [8,9] showed that all phosphorites from this largest basin were formed through the replacement of biogenic remains by calcium phosphate. Specimens with broken and polished surfaces were investigated. The best results were obtained when the surfaces were treated with 3–7% hydrochloric acid for 2–4 min. However, it is necessary to keep in mind that the parameters of the treatment are averaged, and an individual approach is required for each actual instance in order to obtain good results.

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Figure 1. Preservation of cyanobacteria filaments and pseudomorphs of purple bacteria (at the right) in the Low Cambrian phosphorites, Khubsugul, Mongolia.

Khubsugul phosphorites are composed of small (tens to hundreds of microns) micronodules representing aggregates of phosphatized fragments of cyanobacterial mats, pseudomorphs after purple and other bacteria, micro-oolites, and microstromatolites. In many cases it is possible to observe the perfectly preserved fragments of fossil cyanobacterial mat and different types of preservation of cyanobacterial filaments and bacteria. As a rule, cyanobacterial filamentous forms of different diameters are associated with rounded, spindle- and dumbbell-shaped bacteriomorphs (Fig. 1). The morphology, sizes, modes of interconnections, and division into cells of filamentous forms suggest that the filaments are most similar to the modern cyanobacteria Microcoleus. The forms of similar sizes from ancient deposits were described by Knoll et al. [10] as an independent genus Syphonophycus. Several species of this genus were described [9,10]. Depending on sizes present, coccoid– and dumbbell–shaped forms represent either cocci of cyanobacteria (up to 10 μm in diameter) or purple bacteria (~1 μm). Sometimes we can observe empty tubes after trichomes of cyanobacteria (Fig. 2). There are walls of cyanobacterial filaments replaced by purple bacteria. The thickness of the filament wall is equal to that of one layer of purple bacteria, which replaces the filament. Sometimes phosphorites nodules are built by fragments of stromatolites. Data on geology, paleontological remains, and paleogeography of the region suggest that the Early Cambrian Khubsugul basin represented a shallow-water gulf or strait with a weak hydrodynamic regime. Cyanobacterial mats formed by filamentous cyanobacteria and purple bacteria inhabited the basin. The mats became intermittently phosphatized under favorable conditions. Owing to the high rate of the phosphatization, the fossil microorganisms are perfectly preserved in these phosphorites. Abundant phosphatized cyanobacterial mats and bacteriomorphous bodies were also found in the Karatau and South China phosphorite deposits. Like the Khubsugul phosphorites, Lower Cambrian Karatay phosphorites consist of micronodule concentrations. The micronodules are composed by phosphatized oncolites or stromatolites, fragments of phosphatized microbial mats, and sometimes of the phosphatized remains of small invertebrates. Microbial mats are mainly built by spherical and dumbbell bacteriomorph forms; tubular remains are found less frequently (Fig. 3) [11]. The role of cyanobacterial mats in the formation of younger phosphorite deposits is no less significant. For example, the enormous Phosphoria basin existed in the Early Permian

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Figure 2. Micronodule from concentration of pseudomorphs of bacteria and with empty tubes from cyanobacteria filaments. Sample from Low Cambrian phosphorites, Khubsugul, Mongolia.

Figure 3. Dumbbell-like pseudomorphs of bacteria in the Low Cambrian Karatau phosphorites, Khazakstan.

in western North America [12]. Although formed mainly through the phosphatization of sponge colonies, the phosphorites of this basin contain abundant fragments of phosphatized cyanobacterial mats and oncolites. Among the cyanobacterial mats there are coccoid bacteriomorph forms and tubes from cyanobacteria. Most likely, the environments of sponge colonies and cyanobacterial mats were similar [11,13]. The extensive phosphorite basins of Cretaceous, Paleogene, and Neogene ages, which are known in North Africa, the Near East, North and South America, Sakhalin, and other regions, also contain many fragments composed of phosphatized cyanobacterial mats and bacterial assemblages [11]. In the widespread Jurassic-Cretaceous deposits of the East-European platform, there are concentrations of phosphate nodules sometimes forming deposits of industrial importance. A lot of nodules consist of massive phosphate microbial mats [14,15].

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Figure 4. Microorganism bodies at the cross sections of Cambrian brachiopod valves Linnarssonia rowelli Pelman from Low Cambrian deposits (Sinian Formatian) of Siberian platform, river Lena.

In some cases, the phosphorites have a continental, fresh-water origin. Continental phosphorites were described by Shkolnik and Zhegallo [16] from the Upper Cretaceous deposits of the Amur region (Far East). They were accumulated in the alluvial-lacustrine conditions. Like the sea phosphorites, the continental phosphorites are mostly composed by phosphatized microbial communities. Microorganisms include cocci, filaments, and rodlike forms. Occasionally, surfaces are covered by a thin film, sometimes with a fine net, probably phosphatized glycocalyx. What is glycocalyx? Recent cyanobacteria have different and frequently slimy covers. The thickness of slimy covers usually increases in unfavorable conditions. The secreted slime forms thin films around cyanobacteria trichomes, which are called glycocalyx (from acidic polysaccharides). The glycocalyx serves to protect the cyanobacteria trichomes. It is preserved in fossil as thin films with small holes. In early diagenesis, the films were mineralized, holes inside them were formed during mineralization with water loss. The land conditions were more changeable than sea ones and glycocalyx developed more intensively. It has been concluded that the chemogenic phosphorites do not exist [17]. Similar types of preservation of phosphatized bacteriomorph structures are demonstrated by shells of ancient Brachiopods with phosphate skeletons—Inarticulate (or Lingulata) class. The shells of Lingulata are built by alternation of mineral, organic-mineral, and organic layers, arranged in parallel to the external surface. The mineral and organic-mineral layers are pierced by thin pores. Organic threads penetrate into the pores from inside. The mineral layers are composed by apatite and close frankolite. The combination of organic matter and thin crystallite apatite in brachiopod shells is probably responsible for the fast mineralization of microorganism bodies after their death. Bacteriomorph bodies were observed at the cross sections of many lingulate valves from sands and the carbonateterrigenous and terrigenous-carbonate sediments of Cambrian [18]. All observed bacteriomorph body valves are spherical or dumbbell forms, sometimes they are rod forms or resemble a mace. Their sizes do not exceed 1–2.5 μm. In some cases, it is possible to see thin threads of phosphatized organic matter connecting bacteria bodies with the valve (Fig. 4). Most likely, they are phosphatized biofilms seen inside the shells of Cambrian phosphate brachiopods; redistribution of phosphorus in the shells being connected with activity of some bacteria [18].

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Conclusion Remains of microorganisms (bacteria, cyanobacteria, and products of their metabolism as stromatolites, oncolites, or biofilms) may be found in phosphorites of every age. Phosphorites can have the sea- or fresh-water origin. Sometimes, phosphatized remains of microorganisms are enclosed in the phosphate skeleton of invertebrates. The main type of preservative of microorganisms is either pseudomorphs of calcium phosphate on bacterial bodies or thin mineralized biofilms. These materials provide excellent models that could be used for the recognition of biomorphic structures in astromaterials.

Acknowledgments This study was supported by the Russian Foundation for Basic Research (projects 00–15– 97764, 02–04–48094, 00–05–64603).

References [1] Rozanov AYu, Zavarzin GA. Bacterial paleontology. Proc. SPIE 1998; 3441: 218–21. [2] Abysov SS, Walsh M, Westall F, and 15 other authors. Bacterial paleontology. M: PIN RAS 2002; 1–188. [3] Gerasimenko LM, Goncharova IV, Zavarzin GA, Zhegallo EA, Pochtareva IV, Rozanov AYu, Ushatinskaya GT. Dynamics of release and absorbtion of phosphorus by cyanobacteria. Ecosystem restructions and the evolution of biosphere. Moscow: Nedra 1994; 1: 348–53. [4] Gerasimenko LM, Goncharova IV, Zhegallo EA, Zavarzin GA, Zaitzeva LB, Orleansky VK, Rozanov AYu, Ushatinskaya GT. Process of mineralization (phosphatization) of filamentous cyanobacteria. Lithol. and Min. Resources 1996; 2: 208–14. [5] Gerasimenko LM, Hoover RB, Rozanov AYu, Zhegallo EA, Zhmur SI. Bacterial paleontology and studies of carbonaceous chondrites. Paleontol. Journ. 1999; 4: 103–25. [6] Ilyin AV. The Khubsugul Phosphorite Basin. Moscow: Nauka 1973; 1–167. [7] Yanshin AL, Zharkov MA. Phosphorus and potassium in nature. Novosibirsk: Nauka 1986; 1–189. [8] Rozanov AYu, Zhegallo EA. Problem of origin of the ancient phosphorites of Asia. Lithol. and Min. Resources 1989; 3: 62–82. [9] Zhegallo EA, Rozanov AYu, Ushatinskaya GT, Ragozina A, Gerasimenko LM, Hoover RB. Atlas of microorganisms from ancient phosphorites of Khubsugul (Mongolia). Huntsville, Alabama: NASA MSFC: 2000. p. 1–167. [10] Knoll AN, Swett K, Mark J. Paleobiology of a Neoproterozoic tidal flat/lagoonal complex: the Draken conglomerate formation, Spitsbergen. J. Paleotol. 1991; 65(4): 531–70. [11] Shkolnik EL, Tang Tianfu, Eganov EA, and 8 other authors. Nature of phosphate grains and phosphorites from the largest basins of the world. Vladivostok: Dalnauka; 1999. p. 1–207. [12] McKelvey VE. Phosphate deposits. U.S. Geological Survey Bulletin 1967; 1251: D1–D123. [13] Shkolnik EL, Zhegallo EA, Eganov EA. About origin of phosphate grains (pellets) from phosphorites of Formation Phosphoria, USA. Lithol. and Min. Resources 1992; 5: 126–33. [14] Shkolnik EL, Zhegallo EA, Eganov EA, Bogatyrev BA. Biogenic structures in bauxites from some localities in Russia, Brazil and India (results of electron microscopy). In: Mineralogy and life: biomineral homologies. Syktyvkar; Geoprint 2000: 125–7. [15] Shkolnik EL, Zhegallo EA, Krasnov AA. The biomorphic types of Mesozoic nodules of East-European platform. In: Mineralogy and Life: Biomineral Homologies. Syktyvkar; Geoprint 2000: 44. [16] Shkolnik EL, Zhegallo EA. The studying of continental phosphorites from town Blagoveschensk, Amur district with electronic scanning microscope. In press. [17] Zhegallo EA, Rozanov AYu, Ushatinskaya GT. There are not chemogenic phosphorites! International Symposium Problems of Phosphate Geology, Moscow: IM-Bisbess Abstracts October 17–18 1995; 13. [18] Ushatinskaya GT. The earliest lingulates. Moscow: Nauka; 1995. p. 1–91.

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Recent Microbiology and Precambrian Paleontology Georgy A. ZAVARZIN Institute of microbiology Russian Academy of Sciences, Moscow 117312, Russia Abstract. The study of possible astrobiological and ancient terrestrial biospheres might be based on an actualistic approach. The survey of relict microbial communities and their habitats demonstrates that actualistic microbial biogeochemistry might bring light to the early biosphere if it is based on the data from Earth sciences, which comprise the larger system. Scaling is the key issue for systemic approach. The general features of relict microbial communities, which are found in extreme habitats such as hydrotherms, hypersaline lagoons, and soda lakes, are described. They conform to demands for autonomous communities with closed biogeochemical cycles. Incomplete cycling leads to the biogeochemical succession. Reconstruction from actualistic studies should be based on the firm base of the paleorecord, obtained by geologists from the field studies of ancient rocks and the empirical data of microbial paleontology.

1. General Background The main problems in the study of Precambrian life are the questions, how accurate is the knowledge of recent processes, and to what extent is the principle of analogy applicable to an ancient environment? The same questions arise when the problems of extraterrestrial life are discussed. In this approach, an operational definition of life is needed, which is given in two theses: (1) Life is an emergent feature of the system of events, and (2) life is a discrete phenomenon represented by organisms. From those two postulates, it follows that there can not be a phenomenon of life as a feature of single substance, and so-called molecular biology is a misleading metaphoric term, i.e.: life ends with the descent to the molecular level, and the field of chemistry begins. The usual question about viruses is withdrawn because they produce features of life only when included in organisms. Outside the organism viruses have features of chemical particles, which can crystallize. Life cannot be envisaged as a homogenous (soup approach), rather, it is heterogeneous (pelmeni or tortellini). Life is represented by organisms, i.e.: the interacting system of components, which can exhibit their features in artificial medium but cannot proliferate without interaction with other components. Four main components should be taken in account: (1) replisome with DNA, (2) ribosome with RNA, (3) membrane with energy-yielding ATPase, and (4) cytoplasm with proteomic metabolic pathways. From interrelation between the parts of a prokaryotic cell, it is evident that the components of the system are interdependent, and thus, make an entity of simplest organism (Fig. 1). The crucial stage is the emergence of life from the components of a future organism. It might be tested by reverse experiment by the rearrangement of an organism from its parts. That has never succeeded, so attempts to substitute the origin of life by the origin of chemical substances are irrelevant to the problem.

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Figure 1. Interaction of the components within simplest organism [1].

Analysis of the system might be done by two ways: (1) from the bottom up or (2) top down, i.e.: from the element to the system or from the system to its elements. Typical analysis of biological systems from the bottom is given in a hypothesis of RNA-world. Here the opposite route is tried: top-down analysis from the whole to its parts. That method is the usual reductionism pathway, which dissects an entity to its parts. On this pathway three hierarchical levels should be considered for each step: (1) system, (2) subsystem or component, and (3) element. Subsystems, or components, depend on compatibility with the system. Components that are not compatible with the system are excluded. The only features of the component that are significant to the system are the features that interact with other components within the system. The same is true for the elements within the subsystem. The goal of the system is its sustainability. Suggestions to the contrary are obviously absurd since such systems would disappear spontaneously and, therefore, should not be considered. In biology, no species (element) can exist outside the community (component) in the biosphere (system) for a geologically significant time. This thesis was proposed by Vernadsky in the late 1920s, but it should be noted that Earth as a huge organism was envisaged by Winogradsky [2],1 discoverer of chemosynthesis and thermodynamic limitations of life in his lecture on “The role of microbes in the cycle of life” at the Imperial Institute in St. Petersburg in 1896, which is the date for the beginning of global microbial ecology. The community forms a sustainable entity from the elements, with the main links between its components, i.e.: physiological groups of species with similar metabolic functions, represented by trophic interaction. These interactions are organized in the metabolic network pathways in the community in a way similar to metabolic pathways in the cell. The metabolism of a community is organized in a cyclic pathway so that the initial substrate accumulated in the biomass by anabolic autotrophic processes at the expense of external energy is completely decomposed into the product, which is the same as the substrate, mainly carbon dioxide (CO2) is supposed. Microbiologists use the word mineralized, which should not be used in the frames of paleomicrobiology. Only communities with a closed cycle of matter, balance of biogenic macroelements, could be considered autonomous and sustainable. Prokaryotes form such a functionally complete community. Imbalance of matter can occur either locally or temporally leading to accumulation of the products. Imbalance is a moving force of succession. On the global scale, succession is a driving force of irreversibility and biogeochemical evolution. Diversity of organisms retains ancestors as well as their complex descendants. On the geospheric-biospheric scale, all diversity of evolutionarily different organisms is observed. Reconstruction of the universal phylogenetic tree from the similarity of sequences in informational macromolecules in recent organisms supposes that random mutations only slightly changed the ancient progenitors. This means that they are persistent in spite of evolution. The question is why.

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Descendants can survive only if the ancestral system, which existed at the moment of their appearance, is retained. The opposite supposition, that newcomers are adapted to the future, is meaningless. That would mean that evolution occurs on the superpositional principle, i.e.: additive evolution [3]. Combinatorial and additive evolution occurs in a nonDarwinian cooperative field while Darwinian substitutive evolution by competition is found within the functional component. For instance, a partial substitutive sequence is found for prime producers, such as cyanobacteria, algae, and plants, which comprise the trunk of the evolutionary tree by initiating an organic carbon (Corg) cycle. Superpositional evolution makes evolution possible by the loss of functions performed by an ancestral system. The stability of ancestral systems indicates that ecosystems could be found now, which are analogous to the communities of the past, primarily for microbial communities of the Precambrian prokaryotic biosphere. These communities might be designated as relict communities. Refugia for such communities are found in extreme conditions. Microbial communities of extremophiles develop in sites where eukaryotic organisms are absent or appear as occasional invaders. The existence of relict microbial communities indicates that the basis of life shrinks with an increase of complexity. Extremophilic communities are most important for astrobiology because they indicate the limits of terraforming life and the corridor of habitability. Habitability precedes the habitation, means that the geosystem is primary and the biosystem is secondary and dependent. The science of geophysiology is a metaphoric expression for some transformations carried by biota not always for its own profit. Biogeochemical succession from an anoxic to an oxygenic environment in the Proterozoic is the obvious illustration. Paleomicrobiology, in spite of all difficulties in interpretation, gives an empirical basis for understanding the evolution of the geospheric-biospheric system in Precambrian. Biotic cycles depend on the cycle of Corg with an autotrophic productive, branch CO2+H2O= [CH2O]+O2, and an organotrophic reverse reaction of destruction. The cycle of Corg is linked to the cycles of nitrogen (N2) and phosphorus (P) by the anabolic ratio, Corg:Norg=6 and Corg:Porg=106, representing the ratio of these elements in biomass. Destruction represents a regenerative cycle, which replenishes the major biogenic macroelements, phosphorus and nitrogen. Due to the ability of prokaryotes to the energy-consuming nitrogen fixation, recycling of nitrogen is not as crucial for the cyanobacterial community as it becomes in the eukaryotic world. Some excessive Corg escapes recycling and, via recalcitrant Corg compounds, enters the pool of sedimentary reduced carbon (C2) with kerogen as the main substance. The inability of microbes to complete the destruction of mortmass, primarily in anaerobic environment, leads to oxygenic biogeochemical succession in the history of Earth. Cycles of sulfur (S) and iron (Fe), as well as the nitrification portion of the nitrogen cycle, are catalyzed by chemosynthetic (chemolithotrophic) bacteria. The general rule is that lithotrophs develop in the domain of the Eh-pH stability of the products of the reaction if its thermodynamic is sufficient to fulfill ATP formation [4]. The sulfur cycle operates in full strength now, and the iron cycle was important in Proterozoic living deposits of iron oxides as banded iron formations. In biologically mediated reactions, the domains of Eh-pH stability for different minerals are reached as the result of microbial activity, usually as byproducts in Corg. The most important among reactions mediated by microbes is the calcium (Ca) cycle with the leaching of rocks by CO2 and acids produced by the decomposition of Corg and the precipitation of carbonates as documented by stromatolites. The calcium cycle in Precambrian is most important in the weathering-sedimentation set of processes and the burial of atmospheric CO2 in carbonates [5]. Since the Cambrian, calcium recycling involves direct formation of carbonates inside compartmentalized eukaryotic cells under the action of carbanhydrase. Another example of a biotically mediated reaction is non-specific oxidation of reduced com-

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pounds by active oxygen (O2) species produced during respiration and catalyzed by peroxidases. Diagenesis in the sulfidogenic zone is another example of reactions mediated by microbes. Less understood are the microbe-mineral interactions in diagenesis. As a general assumption one should consider formation of amorphous colloid precursors with subsequent non-biotical crystallization, which makes a barrier to rapid microbial transformations.

2. Relict Microbial Communities as the Models for the Past Microbial communities are organized toward universal frames of trophic network. The general scheme of trophic network is applicable for microbial communities developing in different habitats with variations depending on the topic conditions, such as temperature, salinity, alkalinity, etc. In anaerobic degradation, two alternative pathways are possible: (1) methanogenic, prevailing at low mineralization, and (2) sulfidogenic, at high mineralization, predominantly in the sea. The aim of microbiologists is to understand microbial diversity within functional components of the trophic systems of different habitats and fill up rectangles with the names of microbial species. Winogradsky’s rule of microbial ecology should be taken in account: each natural compound has its specific decomposer [2]. The trophic scheme, below (Fig. 2), is a guide for the study of recent microbial communities and, by analogy, for the reconstruction ancient ones. In the scheme, links to O2 and CO2 are not indicated. It should be mentioned that the scheme is quite simplified, and many pathways are omitted. It is clear that a microbial community acts as an entity with energy balance for the whole system, as it is within the metabolizing cell. However, in community each step must be sufficient for supporting the life of a microbial species. Most indicative is interspecific hydrogen (H2) transfer by syntrophs, which allows their development only if the H2 pressure is kept low by hydrogenotrophs.

Figure 2. Generalized version of trophic network for the cyano-bacterial community, where cyanobacteria represent prime producers, and bacteria—destructors. Three sets of objects are to be considered: (1) functional groups of microbes (rectangles), (2) chemical compounds (ovals), and (3) flows (arrows) representing both trophic interdependence and material transport processes. Note: dissolved organic carbon (DOC) and volatile fatty acids (VFA) as products of fermentation. Phototrophs utilizing light energy are in bold letters [5].

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To what extent might knowledge of recent microbes bring light to the ancient processes? There are two alternative answers. The first is that there is nothing new under the Sun, in spite of its lower luminosity in the past, and at full strength, the actualistic approach can be used. The second is that the irreversible geological processes and the increasing diversity of biota limit the actualistic approach. The real problem is that one cannot think without using the principle of analogy and comparison with something already known. An attempt to search for life on Mars, avoiding any Earth-based experience and looking, for instance, for morphological complexity of images might produce results that will not convince skeptics because they have no equivalent concepts in their mind, and it takes time to create new concepts. Fortunately, in the Earth study, the aim is to find the roots of known plants. The careful investigator will probably base judgments on things that are known and try to consider limitations for the application of knowledge to the misty field of the past, which means that the comparative mode of thinking will prevail. Understanding what was on ancient Earth might be done by the reconstruction of extinct groups of organisms known from paleontological record and the reconstruction of their mode of functioning by comparison with a few recent representatives from the same group. That is the method of actualistic paleontology based on comparative approach. When there is a need to understand, not a single species or type of organization, but an overall picture, paleobiology is the appropriate arena. Here, a reconstruction of paleolandscape is needed, and biologists should work together with geologists. The easiest situation is when it is possible to reconstruct the paleolandscape by comparison with something similar on modern Earth. Communities that inhabit such landscapes might be classified as relict if there are good fossils analogous with the past. Microbes do not need hills and valleys; they suffice themselves with microhabitats. Such natural mesocosmos might be found in nature. The problem is to eliminate the influence of things, which were absent in time to be reconstructed. For modeling the Precambrian, things to be eliminated are primarily the influence of plant cover and the soil as a root-inhabited layer, which changed the subaerial surfaces. Thus, extreme conditions where plants do not grow and animals do not crawl are required. Astonishingly there are many such habitats where only bacteria can survive due to the temperature, high salinity, alkalinity, anaerobiosis, or simply because of the space in the porous media of the rocks. From this well-known fact of the high tolerance of bacteria, comes conclusion that with the increase of complexity, which is the main characteristic of biological evolution, the base of life is shrinking and attained complexity leads to functional degeneration. The idea was called “evolution of lost functions” by Andre Lwoff [6]. What is called “normal environment” is only a sector of various conditions exploited by biota in the past and evidence of shrinking abilities. The question not only concerns the fitness of recent biota to the modern environment but also the creation of this environment by the evolution of the geosphericbiospheric system, which was produced by them in the past. Study of the relict microbial communities gives a possibility to visualize the ancient biosphere, not as virtual one, but by real pieces of it. The bacterial biosphere dominated until the Neoproterozoic revolution ~800 Ma ago with its transition to the bacterial-protista biosphere, exemplified now largely by the oceanic system [7], and then to the soil-plant cover dominating the terrestrial ecosystem, which appeared only after 480 Ma ago [8,9]. Before that time, Prokaryotes were sufficient to establish the mode of geosphere-biosphere interaction making a precondition for the future biotic evolution. But, one should be most careful in applying the actualistic principle to the Archaean, however, not excluding possibility of life of certain types of bacteria and their communities similar to the recent. Most probably it might be applied to the hydrogenotrophic microorganisms of the deep biosphere using endogenous H2 in chemosynthesis. However they do not represent the main trunk of evolution on Earth.

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3. Additive and Combinatorial Evolution of Biota In the course of time, new species appear and some old ones become extinct. The survival of the fittest is the central concept of evolutionary biology, which can be defined as substitutive. This line is confirmed by paleontology, although more in terms of increasing complexity than functional fitness. If temporal and spatial scales are changed, different conclusions appear. The entire geospheric-biospheric system with its functional components, rather than a set of indicative species used by stratigraphs and in textbooks, should be considered. As a result, not an origin of the species but the evolution of communities comes into the focus. The functional organization of a community system is cooperative. Functional organization is unrelated to the phylogeny of its elements. Communities of functionally diverse organisms form a cooperative entity that conforms to the environment. Cooperation in communities is mainly performed by the trophic interactions. It is an empirical rule, first recorded by Zavarzin [10] for the anaerobic community of decomposers, that most close trophic interaction occurs between phylogenetically unrelated or even extremely distant organisms. A striking example is in the biotic cycle of methane (CH4) (Soehngen cycle) were methanogenic archaea interact with methanotrophic proteobacteria from one side and receive their substrates, H2 or acetate, from various anaerobic organotrophic bacteria, which means that the community is non-monophyletic in its origin and is constructed by recruitment from the outside. Within the components of the system, species with similar functions can substitute for one another by competitive selection. This interaction or even interdependence evolves by the recruiting of the functionally needed organism from outside, not by the divergence from the common ancestor. That means that on this level, fitness for the environment develops by a combinatorial process. Stepping down to the genetic level, it becomes clear that the combinatorial process in prokaryotes should be considered as some kind of lateral gene transfer [11]. An example of such an evolutionarily late process might be given for the cellulolytic organisms. They are dispersed over various phylogenetic branches, and molecular analysis of cellulases forced Doolittle [11] to accept lateral gene transfer as a major process for this group of enzymes. For instance, in the halophilic community within Order Haloanaerobiales, there is cellulolytic Halocella, which obviously obtained its cellulase only recently for feeding on mortmasses of Cladophora sivashensis [12]. Phenotypic diversity of morpho-physiological genera known in 1970s represented a network or combinatorial matrix in space of logical possibilities for characters excluding forbidden combinations [13]. The development of communities occurs via combinatorial processes on an organismal level by recruiting needed allies and by lateral gene transfer on genetic level. Acceptance of the organisms by the community depends on the structure of community. The newcomer must fit into that certain functional role within the community. Functional structure of the community is built from the top down—from possibility to realization [5]. Since the newcomer, regardless of origin, can survive only if it fits into the already existing community, evolution should be additive. That means that major functional diversity should be retained in the course of evolution. Substitutive evolution, illustrated by the evolution of Vertebrates and vascular plants, is not a universal but a partial event. Within the events of substitutive evolution, which is recorded by paleontology, the functional role remains approximately the same. This raises the question about the validity of individual changes as the universal driving force of evolution, but not about its mechanism since changes only occur in the individual. Functionally important is not the origin of an organism and what it inherited from his ancestors but what it does within the community according to the actual geospheric-biospheric system of the present. It is impossible to interact with the past or with the future. The struggle for existence means a struggle for the position within the cooperative entity.

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Figure 3. Geospheric system of Earth [16] energy and catalytic links are designated by dotted lines. Note the key role of atmosphere and CO2 in geospheric processes and the CO2 sink in carbonates, which allows Earth to escape runaway greenhouse effect. The calcium cycle is responsible for the elimination of CO 2 from the atmosphere. Carbonates are balanced by clays formation, which are involved in burial of sedimentary reduced C2. In this scale kerogen, not biomass, balances O2 of the atmosphere.

The challenge to the heretical picture outlined here leads to the search for feedbacks that might change the overall system. In the history of Earth, these changes are evident. These changes are a sequence of prime producers from cyanobacteria to phototrophic protists, then to algae, and then to the plants (Fig. 2). However, one might notice that the more it changes the more it remains the same, with the chloroplasts derived from cyanobacteria integrated into the eukaryotic cell with further development into plant tissues being in the lines of the morphological differentiation. The symbiogenetic hypothesis of Margulis [14] provoked the greatest change in the way of thinking from individual mutations and microevolution to the macroevolution by the systemic changes.

4. Biosphere and Geosphere Interaction There are two main feedbacks from the biota to the geosphere—both caused by the change of the chemical composition of the atmosphere (Fig. 3). The first is caused by O2 production and dissemination into the atmosphere, and the second by scavenging CO2 from degazation. Both are linked to the cycle of Corg. The fate of O2 directly depends on biota, but the fate of CO2 on a geological scale mostly depends on inorganic transformations caused by the biologically mediated reactions. The changes of atmospheric composition are the functions of microbes, which can transform most components except for inert gases [15]. It is accepted that, around 2 Ga, the atmosphere became oxygenic with free O2 and everything changed from anaerobic to aerobic. This is not exactly true since, from the very first appearance of oxygenic photosynthetic cyanobacteria, their cohabitants in a microhabitat should be either oxytolerant or facultatively aerobic during the day time, switching their metabolism in the course of hours. Nevertheless, ~2 Ga ago there was a reservoir of atmospheric and dissolved O2 large enough to support an aerobic way of life even during the nighttime.

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That brought a great relief to photosynthetic organisms, which could use their storage compounds not by lactic fermentation as cyanobacteria do, but by aerobic respiration and by the use of lipids as another kind of storage. The way for increasing body dimensions was opened. What was the real cause for O2 accumulation in the atmosphere? In the dimensions of the geospheric-biospheric system, free O2 is an equivalent to unoxidized Corg. That is the imbalance in the production-destruction cycle, which causes accumulation of undecomposed organic matter and the equivalent accumulation of photosynthetic O2. On this scale one should look not only at the productivity, but also at the block in decomposition as precondition for O2 accumulation. The real reason for O2 evolvement from the ecosystem is the inability of decomposers to oxidize all Corg produced. The main route for Corg to escape decomposition on the geological scale is burial in the sedimentary rocks as kerogen. Thus, it is the rate of sedimentation that is responsible for the formation of the oxygenic atmosphere. Kerogen is present in the sediments in two forms: (1) as carbonized remnants of the organisms, part of which could be recovered as so-called organic-walled microfossils, and, (2) as amorphous humic substances in films associated with the mineral particles [17]. Reduced C2 content varies with the type of sediment, being higher in the fine deposits of clays, but it is astonishingly high, even for the oldest sedimentary rocks. As a result, the conclusion is that the geospheric system, as the larger system, dictates to the biospheric system, i.e.: the direction of development is from the top down. The rate of sedimentation depends on tectonics, relief, and atmospheric hydrological cycle, but in essence, the subaerial weathering on continents is the driving force. That is different from the evolution of biota caused by individual changes, and on the next step from the Gaian idea of the biota establishing an environment for its own purposes. Biota is under the pressure from the larger system. Negative feedbacks are a feature of any sustainable system. Without such feedbacks, a system cannot exist; however, these feedbacks are not absolute and as has been seen with the most impressive example of O2 production, which changed the entire geospheric-biospheric system, the incomplete efficiency of feedbacks leads to the biogeochemical succession, which is the main driving force in the evolution of the geosphericbiospheric system [5]. The key word is succession, not in its usual botanical sense of reversible process, but as a sequence of irreversible events on a large scale.

5. Distribution of Relict Microbial Communities Relict microbial communities might best be located on the imaginary platform drifting accordingly to the mobilist concept (Fig. 4) [5]. This picture is not applicable for Archean communities but indicates positions where local sites for relict microbial communities might be found now. Active margins give a place for volcanic activity with hydrothermal springs and emissions of endogenous gases. An important reaction is the deep seepage of meteoric water and its return as a steam after reaction with superheated rock, making hydrological cell in hydrotherms. Spreading centers in the deep ocean involve convective cells of seawater reacting with heated basaltic rocks and bringing up reduced metals and sulfides. A passive margin is the site of sediment accumulation in marginal seas, forming hypersaline lagoons, where evaporitic processes dominate in arid climates. The intracratonic part is the site of subaerial weathering with soda lakes in endorheic regions and watersheds of rivers in humid climates. Subterranean, deep biosphere, is of secondary importance in the terraforming process, but it is obviously the most important for astrobiology. It is best studied for volcanic hydrotherms and deep oceanic vents. Hydrotherms are formed by water cells when water seepage from the surface (not juvenile water) comes in contact with superheated rocks, usually

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Figure 4. Distribution of relict microbial communities on a simplified platform.

~3 km under the surface and under high temperature and pressure, and is transformed into fluid bearing reduced compounds and, particularly, H2. Superheated vapors rise and reach the zone of condensation at a lower temperature. For Earth, the zone of condensation is above 100 ˚C. From that point to the surface, begins the habitat of hyperthermophilic microbes. In this reducing environment, the problem is in oxidants, which are sulfur or CO2. The preferred donor is H2, and many hyperthermophiles belong to hydrogenotrophic sulfurreducing Crenarcheota. The reduction of CO2 leads to hyperthermophilic methanogenesis by Euryarcheota. If one considers hyperthermophilic chemosynthetic microbes from the deep biosphere as the most ancient community of organisms utilizing energy from endogenous sources, one is forced to limit their metabolic possibilities by hydrogenotrophic anaerobes. The problem is how to scavenge H2S and methane as the major products of metabolism in anoxic biosphere. H2S may be oxidized in anoxygenic photosynthesis with production of sulfate in a purple ocean, however, phototrophic anoxygenic H2S oxidation is not observed in thermophilic communities. Oxidation of methane is more difficult, but an anaerobic syntrophic process might be supposed for the oxidation with sulfate. In contemporary thermal habitats, when streams of gases and vapors reach the surface, convection brings allochtonous organic matter in thermal fields and in shallow waters providing the possibility for the development of proteolytic archaea. In deep-sea vents, O2 is brought in by convection and an aerobic chemosynthetic deep-sea oasis develops [18]. These habitats are secondary, and for astrobiology, the most important is chemosynthetic subterranean biocoenosis. The pathway for the elimination of reduced compounds by bacterial oxidation in an O2 atmosphere is obvious. Hydrogen is oxidized aerobically by the phylogenetically oldest bacteria from extremely thermophilic Caldobacterium-Hydrogenobacter-Aquifex and Caldithrix groups. The same route of aerobic oxidation could be suggested for sulfate production by Sulfolobus type microbes. The main problem with chemosynthetic hyperthermophiles is the fact that they do not represent the stem of biological evolution on Earth. In the depth of thermal fields, a zone of condensation of thermal fluids begins around 100 ˚C, depending on pressure. Porous space of volcanogenic sediments is the habitat for hyperthermophiles, mainly sulfur reducing. The number of microbes in the porous space is very high, ~105 per gram of rock. Many of them are archaea, which utilize H2 and polymeric organic substances and produce H2S; Stetter and his group extensively studied this group and thoroughly reviewed it. The question is from where do the archaea obtain polymeric organic substances? A soup of boiled organic is transported to the sites of thermophiles development by a convective stream of water enhanced by the injecting force of a

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gas stream, e.g.: cellulose-decomposing Anaerocellum (reclassified afterwards as Caldocelluloseruptor and extensively studied) [19]. Of course, no cellulose-producing organism can develop at 70 ˚C. But, the site of isolation was a griphon under a hortensia bush and the bottom of the hotpot was filled with leaves. This is an example that one should take the sample by one’s own hands and consider peculiarities of the habitat for further interpretations. One of the most striking things on solfataric fields is the high acidity and resulting decomposition of igneous rocks into clays. Sulfuric acid is formed due to activity of aerobic sulfur-oxidizing microbes and depends on availability of O2. The main part of sulfuric acid is formed at ambient temperature by mesophilic thiobacilli. High acidity on the steaming parts of a solfataric field is caused by the evaporation of an acidic solution. The role of mesophilic thiobacilli, as the source of sulfuric acid, was quantitatively demonstrated for Uzon caldera [20,21] and afterwards to Yellowstone; however, long before Humboldt and Gay-Lussac discovered that the acidity was not caused by hot volcanic exhalations but by the cold walls of the Vesuvian crater. Of course, there is a most interesting community with many archaea developing in boiling acidic mud pots and producing sulfuric acid as Sulfolobus found by T. Brock [22], but the simple physical mechanism of evaporative concentration escapes attention of biologists. The most characteristic lithological patterns of sulfuric acid weathering might be used as an indication for O2 in paleostudies. Subaerial light-dependent thermophilic microbial cyano-bacterial communities develop in hot springs and might represent the key community in a terraforming process. They proliferate not only because of light energy and fresh nutrient input but also using reduced endogenous exhalations. These exhalations imitate the ancient atmosphere with a lot of CO2 and some reduced gases. Thermophilic communities were studied in Yellowstone, California and much less in Iceland, which represents another type of volcano [22]. Extensive studies of thermophilic cyanobacterial communities from Kamchatka demonstrated that at 65 ˚C and with a stream of CO2 dominating volcanic gases, a microbial community with a complete trophic network proliferates [23]. It changes the gas composition of exhalations by the oxidation of reduced compounds, such as the H2 and sulfur species. The transformation of volcanic gases by thermophilic cyanobacterial mat dominated by Mastigocladus demonstrated that gas mixtures were transformed into something like air with somewhat more than 20% O2 marking the upper limit. Reduced gases are completely oxidized by thermophiles with the remarkable exception of methane. These experiments clearly illustrate the ability of cyanobacterial communities to transform a primitive atmosphere into an oxygenated atmosphere [24]. Thermophilic cyano-bacterial communities at modest temperatures allowing the growth of cyanobacteria are complete in the sense that all functional groups of decomposers are present with the final part performed by Thermodesulfobacterium for sulfidogenesis and Methanobacterium thermoautotrophicum for methanogenesis, both being described by G. Zeikus at the very beginning of studies by the team of T. Brock [22]. Methane, which not only comes with volcanic gases but is also produced within the thermophilic community by hydrogenotrophic and acetoclastic methanogens, is not oxidized. This inability for the oxidation of methane by thermophilic methanotrophs immediately calls into question Gould’s idea concerning the ancient source of endogenic methane since the way of its oxidation should be found either by photochemical reactions in an anoxic atmosphere or by microbial oxidation. The study of organic matter decomposition by thermophiles indicates that below 80 ˚C, all of the more than 100 compounds tested were decomposed and supported the growth of bacteria. Over 80 ˚C, the number of compounds used by microbes drastically decreased. Thermophilic cyanobacterial communities are a good starting point for the trunk of phylogenetic tree. Organisms from this community are analogous to the mesophiles now living

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at normal conditions. They can catalyse reactions of all biogeochemical cycles of main biogenic elements. One can guess that microbial communities of this type were ubiquitous on Earth before eukaryotic communities in mild environments supplanted them. There is nothing that can forbid cyanobacterial mats to spread over the wet subaerial surfaces of Earth. If this is accepted then projective chlorophyll cover might be assumed approximately constant with annual production n.102 Gt Corg during Earth’s history. The zone of sedimentation is situated on the passive margin of our imaginary continent. Shallow seas were inhabited by cyano-bacterial communities, but now they are exemplified by communities of hypersaline lagoons as the sites of formation of evaporites. Cyanobacteria proliferate up to about 17% salinity, which excludes all eukaryotes except for green unicellular Dunaliella. Halophilic communities of lagoons, represented by cyanobacterial mats, now with domination of Microcoleus, were the objects of extensive studies [25–28]. These types of mats are similar all over the world. They represent rigorously structured, layered community with prime producers on the top and a sequence of decomposers below. Layers follow one another in sequence, physically approximating the trophic chain as it is represented in Fig. 2. This type of cyanobacterial community structure is universal for different mats. Cyanobacterial components of the community are well studied [29]. There are two aspects, which were out of focus. The first is the pathway of mortmass degradation in a mat, which involves the anaerobic halophilic community. In modern thalassic mats, the end of decomposition is performed by a sulfur cycle with the H2S branch catalyzed by sulfidogens and SO42– produced by the purple bacteria, such as Thiocapsa. This way of sulfate production might be considered a possible explanation for the origin of oceanic sulfate in an anoxic purple ocean as an alternative for production of sulfate by aerobic thiobacilli. Ecosystems of the purple type are known now in the Indian Ocean below the zone caused by wind mixing. However, most pathways of decomposition in anaerobic sections of mats are not yet described, in spite of the possibility that some limitations in degradation, for example, of lipids and phospholipids of membranes, might lead to kerogen formation as the source for oil formation. Peculiar pathways in halophilic communities are caused by the degradation of organic osmolithes with haloanaerobes [30] that are involved in decomposition [31]. The second and most important aspect is lithification of the mat. The role of cyanobacterial mats as precursors for the formation of stromatolites is well established. Thus, this is the best example of the actualistic approach and the best use of recent microbial communities to describe the past. Studies of stromatolites and the associated microfossils form the largest body of information in micropaleontology of the Precambrian (Semikhatov and Raaben [32]). The usual idea is that photosynthesis causes the local alkalinization and precipitation of carbonates. Calcium precipitates as thin layer below the active cyanobacterial layer, which is 2- to 3-mm thick. Gradients of light penetration, pH, O2 concentration, and the role of diffusivity are established on microscale by Jorgensen et al. [26]. However, these gradients depend on the slow molecular diffusion in a gel of mat matrix. This limits the inflow of cyanobacterial-bearing water into the mat. Processes of precipitation seem to be sufficient for the enrichment of sediments by phosphates. This sufficiency is proved by laboratory experiments and in the micropaleontological record [33]. However, photosynthetic precipitation of carbonates is insufficient for the lithification of mats into massive rock. All attempts to model carbonate precipitation and, particularly, cementation caused by photosynthesis were unsuccessful. The lithification of a mat might occur as a sedimentary process on the alkaline geochemical barrier of larger geographic dimensions than microgradients caused by photosynthesis. Oceans may be supposed as reservoirs of Ca2+ and continents as sources of alkalinity. Contact between these two types of water causes the chemical precipitation of carbonates in the mixing zone. Precipitated carbonates settle on mats. This process could be mod-

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eled in the laboratory. When the precipitate is ~1-mm thick, live cyanobacteria glide out and spread over the surface. Repetition of the process leads to the formation of a layered structure closely resembling stromatolites but not solid. The process of cementation is not reproduced here. When enough magnesium (Mg) was present, the sediment at the pH 10 zone had a composition of Ca:Mg=1:1 as in dolomite, but the crystal structures of dolomite were not present. One might suppose that crystallization occurs during diagenesis after the biogenic phase. In model experiments with a cyanobacterial ocean and soda lake, Masticocladus developed in the mixing zone jointly with carbonates precipitation, but live trichomes were moving between mineral particles and were not fossilized. The epoch of dolomite formation is characteristic to Early Proterozoic whereas lime dominates now [34]. The picture of a slightly acidic or neutral ocean interacting with the alkaline waters of continental origin poses the question concerning the origin of alkalinity. The answer is obvious—subaerial chemical weathering by CO2 derived from the atmosphere. The scale of the process was estimated by Kempe and Degens [35], who used the metaphoric expression “soda ocean” to designate amounts of sodium (Na) and were caught by the word and by the impression of great African alkaline lakes and argued for the ocean chemistry [36,37]. However, the mechanism of soda formation is essentially subaerial. This type should dominate over terrestrial biosphere with cations washed out in humid climate and concentrated in endorheic regions. In semiarid climates, large bodies of water are alkaline. Weathering is the most important process for scavenging CO2 from the atmosphere on geological time scale, proceeding mainly as a physicochemical process with the CO2silicate reaction as the central event. This process is needed to diminish the greenhouse effect [38]. Modeling leads to the conclusion that biota strongly enhances the process; otherwise, high temperature and high partial pressure on subaerial surfaces are needed for the elimination of CO2 from the atmosphere as the main terraforming event [39]. Results of modeling indicate that some important things might be omitted or not considered. Biotic enhancement of weathering by plant cover is estimated as sevenfold with a drastic drop of PCO2 at Devonian and a decrease of the temperature [40]. It is true that pedogenic carbonates inherit isotopic C2 ratios from the plants, which decomposed in soils to be the source of concentrated C2 [40]. However, there is a need to look at what type of biota could be on the subaerial surfaces that lead to the paleosoil (Russians would prefer to say, weathered rock) profiles, which according to Retallack [42] are similar to recent profiles. The main course of subaerial CO2 weathering was described as the leaching of cations from the parent rocks into solution, leaving part of anionic components as alumosilicates, stabilized as clays and oxides, such as SiO2 [43]. Important cations are calcium and sodium, which bind CO2 into carbonates. Calcium, at high PCO2, forms soluble bicarbonates but releases half of the CO2 back at a higher temperature when it precipitates as CaCO3 in warm waters. Calcium and Mg precipitation occurred as a primary process in Precambrian, leading to the masses of dolomitic rocks [34]. Before 2 Ga, a large part of carbonates had already precipitated, scavenging endogenous CO2. This is the main process responsible for the neutral pH on Earth, and neutrophilic biota might be regarded as calciophilic. The prokaryotic cyanobacterial cycle is a biologically mediated process, which is influenced by the activity of organotrophic microorganisms producing CO2 from Corg, previously concentrated by autotrophs. Eukaryotes with a calcium-precipitating function are involved in calcium recycling and are out of consideration for Precambrian. However, for the geochemists, the calcium-cycle is the most important. Organic acid production, characteristic to most primary anaerobes, strongly enhances calcium-leaching. Contrary to that, secondary anaerobes, such as sulfate reducers or methanogens, precipitate carbonates [44]. In his analysis of CO2 history during the Early Precambrian and the pressure cooking pot greenhouse hypothesis, Schwartzman [38] characteristically omits the fate of sodium, and Kasting [39] is most ironic concerning the soda ocean hypothesis of Kempe and De-

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gens, which is inconsistent with the high PCO2 and taking into account that low early Sun luminosity could lead to the icehouse. The trick is that, for CO2 elimination from the atmosphere, one needs subaerial weathering, which immediately leads to the substitution of the “soda ocean” by the “soda continent” [44]—both terms being metaphoric. Of course, sodium remains on the terrestrial surface only when and until it is not eliminated from the watershed by the riverside run-off into the ocean. However, transitional conditions of sodium enrichment should prevail in the regions where run-off is insufficient. Minimal runoff occurs in ground waters with a sufficient supply of CO2 from the upper horizons, where CO2 is produced from the decomposition of organic matter by organotrophs from the mortmass. An alternative source is endogenous CO2 since it takes place in ground waters in Africa with the hydrothermal activity. Underground anaerobic alkaliphilic microbiota have been studied very little, and it might be interesting for modeling Martian conditions [37]. A belt of soda lakes is observed throughout semiarid regions, from Big Soda Lake in USA to soda lakes in Central Asia. The formation of soda lakes in semiarid deserts depends on CO2 weathering of bare rocks disintegrated into the sand. Soda lakes are very old environments—such sites are recorded for Archaean [45]. Alkaline lakes are quite diverse in their hydrochemistry and, being situated in the semiarid zone, vary during the seasons and from year to year with weather; however larger lakes are more stable. The general rule comes from Plinius: “Water is such as rocks.” For instance, lakes from the East African Rift depend on volcanic activity. Lakes in Central Asia depend on a cryo-arid climate with winter freezing out the brine and precipitates that might not be entirely dissolved during the melting period. One should be very cautious in interpreting single-sampling results, while monitoring ephemeral habitats has its own limitations. For instance, during three visits to Lake Magadi, Kenya—standard site for soda deposits formation—approximately in the same seasons the lake and its biota could not be observed in the similar recurring states. But, even the alkaliphilic microbiota of soda lakes were not studied, in spite of the fact of unusually high productivity of alkaline lakes with cyanobacterial blooms in the Great African Lakes and eutrophication in the steppe lakes with obvious development of a most diverse microbial community [46–49]. One of the reasons for the eutrophication is caused by the fact that phosphate, originating from carbonatites, is not precipitated in the soda lake water by calcium or by iron since these cations are precipitated in alkaline conditions somewhere before. The absence of calcium excludes the usual mechanism of neutralization by the dissolution of calcium carbonate during the acidification and prevention of alkalinization by precipitation of carbonates. In contradistinction to acid environments, microbial life is luxuriant in alkaline habitats at pH 10.2, even at saturation with soda. Cyanobacteria and purple bacteria make bright blooms at this pH. Bright purples in soda lakes gained attention beginning with the first observation by Issatchenko in the 1920s and then the attention of everybody who looked at this habitat. Jannasch, Truper, and Imhoff [46] studied a group of alkaliphilic purple bacteria first with a typical representative, Ectothiorhodospira, described for Wadi el Natrun. The morphological diversity of alkaliphiles in soda brines detected by direct microscopy is most striking—here are all types of unicellular bacteria, including unusual ones, such as prosthecobacteria, microcyclus-like, flat cells etc. [49]. Alkalinity and pH select alkaliphiles that do not grow at pH 7, but a stronger limitation is caused by mineralization and osmotic stress. At a concentration ~100 g/l, microbial growth occurs on all substrates tested. At a concentration of up to 200 g/l, some essential processes, such as cellulose decomposition, are suppressed. For the Early Precambrian, most interesting is the anoxic pathway of decomposition. This is what has been studied by Zhilina and others for the last decade following verification of the hypothesis [50] that in soda lakes, relict terrestrial communities could be found that differ from the thalassic communities of the conservative

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ocean, slowly changing from its Neo-Proterozoic status. Among alkaliphiles, representatives of all of the main phylogenetic branches of prokaryotes are found. The most diverse are the proteobacteria linked to the cyanobacterial group. Bacilli and clostridia represent gram-positives. Spirochetes are observed in mud and isolated in pure cultures. Alkaliphilic archaea Halobacteriles produce blooms in evaporitic brines. The abundance and diversity of alkaliphiles at low mineralization raise the question of whether it is an extreme or a normal habitat? Another problem is in the mode of bioenergetics in a high sodium environment and a low concentration of protons. It is known that some haloalkaliphiles use a sodium energetic instead of proton translocation. This study of bioenergetics of anaerobic alkaliphiles demonstrated that both types are utilized—homoacetic bacterium Natroniella produced ATP at H+- impulse, but hydrogenotrophic sulfate reducer Desulfonatronum at Na+ impulse [51]. All other types of microbial energy metabolisms are recorded among alkaliphiles— substrate phosphorylation in Spirochaeta and arginine decomposition in Tindallia. It might be summarized that diversity of bioenergetics among alkaliphiles covers all known energy producing chemotrophic processes, in addition to phototrophic processes. A survey of the relict microbial communities and their habitats demonstrates that actualistic microbial biogeochemistry might bring light to the early biosphere if it is based on data from Earth sciences. However, reconstruction, giving an understanding of the possibilities, should be based on the firm basis of the paleorecord obtained by geologists from the field studies of ancient rocks and the empirical data of microbial paleontology.

Endnote 1.

“...microbes are the major agents of the cycle of matter called to existence by life and indispensable to regular changes of life....In such a conjunction of events all living matter comes before our eyes as an entity, as a single huge organism, taking its elements from the reservoir of unanimated nature, expediently managing all processes of its progressive and regressive metamorphosis and, in the end, returning all borrowed back to the unanimated nature.” From Winogradsky [2].

References [1] Zavarzin GA, Kolotilova NN. Introduction to environmental microbiology. Publishing House “University”, Moscow (in Russ.) 2001. [2] Winogradsky SN. O roli microbow w obzhem krugoworote zhizni. St. Petersburg: Typography of Imperial Academy of Sciences. 1897. Reprint in English. The cycle of life. Herald of Russian Academy of Sci. 1996; 66(12): 1116. [3] Zavarzin GA. The non-Darwinian domain of evolution. Herald of the Russian Academy of Sci. 2000; 70(3): 252–9 [4] Zavarzin GA. Lithotrophic microorganisms. Moscow: Nauka; 1972. [5] Zavarzin GA. The rise of the biosphere. Herald of the Russian Academy of Sci. 2001; 71(11): 988–1001. [6] Lwoff A. L’evolution physiologique Etudes des pertes des function chez les microorganisms. Paris: Hermann; 1944. [7] Sergeev VN, Knoll EH, Zavarzin GA. First three billion years of life: from prokaryotes to eukaryotes. Priroda 1996; 6: p. 54–67. [8] Kenrick P, Crane PR. The origin and early evolution of plants on land. Nature 1997; 389: 33–9. [9] Meyen SV. Fundamentals of paleobotany. Moscow: Nedra; 1987. 423 p. [10] Zavarzin GA. Microbial community in the past and present. Microbiol. Zhurn. 1989; 51(6): 3–14. [11] Doolittle WF. Some aspects of the biology of cells and their possible evolutionary significance. In: Roberts DmcL, Sharp P, Alderson G, Collins M, editors. Evolution of microbial life. Cambridge: Cambridge University Press; 1996. 1–21 p. [12] Simankova V, Chernich NA, Osipov GA, Zavarzin GA. Halocella cellulolytica gen.nov., sp.nov., a new obligately anaerobic, halophilic, cellulolytic bacterium. Syst. and Appl. Microbiol. 1993; 16(3): 385–9.

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[13] Zavarzin GA. Phenotypic systematics of bacteria. The space of logic possibilities. Moscow: Nauka; 1974. [14] Zavarzin GA. Bacteria and the composition of atmosphere. Moscow: Nauka; 1984. [15] Margulis L. Symbiosis in cell evolution: life and its environment on the early Earth. San Francisco; Freeman: 1981. 419 p. [16] Zavarzin GA. The role of microbiota in rock formation. In: Proceedings of Earth sciences Russian Academy of Natural Sciences; 2001; 7: 131–7. [17] Tyson RV. Sedimentary organic matter. Organic facies and palinofacies. London: Chapman & Hall; 1995. [18] Gebruk AV, editor. Biology of hydrothermal systems. Moscow: KMK Press; 2001. [19] Tikhomirov DF, Stolbova VV, Svetlichny VA, Zavarzin GA. Secretion of the endo-1,4-gluconate cellulase complex by the new extremely thermophilic anaerobic bacterium. Appl. biochem. and microbiol. 1990; 26(2): 252–9. [20] Zavarzin GA, Vasiljeva LV, Trykova VV. On the participitance of microorganisms in postvolcanic processes. In: Proceedings of Academy of Science. USSR; 1967; ser. biol.; 4: 605–11. [21] Karpov GA, Eroschev-Shakh VA, Zavarzin GA. Role of biogenic factors in the formation of environment for the zone of argillization in the contemporary hydrothermal systems and solfataric fields. Volcanology and Seismology1984; 2: 64–74. [22] Brock TD. Thermophilic microorganisms and life at high temperatures. New York: Springer-Verlag; 1978. [23] Zavarzin GA, Karpov GA, Gorlenko VM, Golovacheva RS, Gerasimenko LM, Bonch-Osmolovskya EA, Orleanski VC. Calderic microorganisms. Moscow: Nauka; 1989. [24] Gerasimenko LM, Zavarzin GA. Metabolism of H2, CO2, O2, CH4 in cyanobacterial communities. Microbiologia; 1982: 51(2): 718–25. [25] Cohen Y, Rosenberg E, editors. Microbial mats: physiological ecology of benthic microbial communities. Washington, D.C.: Am. Soc. Microbiol.; 1989. [26] Stal LJ, Caumette P, editors. Microbial mats structure, developments and environmental significance. NATO, ASI Series 1994; G(35). [27] Krumbein WE, Paterson DM, Stal LJ, editors. Biostabilization of sediments. Bad Zwischenahn: Verlag Rosemeier; 2000. [28] Zavarzin GA, Gerasimenko LM, Zhilina TN. Cyanobacterial communities from hypersaline lagoons of Sivash. Microbiol. 1993; 62(6): 579–99. [29] Stal LJ. Cyanobacterial mats and stromatolites. In: Whitton BA, Potts M, editors. The ecology of cyanobacteria: their diversity in time and space. Kluwer: Dordrecht; 2000. 61–120 p. [30] Rainey FA, Zhilina TN, Boulygina ES, Stackebrandt E, Tourova TP, Zavarzin GA. The taxonomic status of the fermentative halophilic anaerobic bacteria; description of Haloanaerobiales ord.nov., Halobacteroidaceae fam.nov., Orenia gen.nov. and further taxonomic rearrangements at the genus and species level. Anaerobe 1995; 1: 185–99. [31] Zhilina TN, Zavarzin GA. Anaerobic bacteria-destructors in the halophilic cyanobacterial community. Zhurn. Obzhei. Biologii 1991; 52(3): 302–18. [32] Riding RE, Awramik SM, editors. Microbial sediments. Heidelberg: Springer-Verlag; 2000. 331 p. [33] Gerasimenko LM, Zavarzin GA, Rozanov AYu, Ushatinskaya GT. Role of cyanobacteria in formation of phosphate minerals. Zhurn. Obzhei. Biologii 1999; 60(4): 415–30. [34] Ronov AB. Osadochnaya obolochka Zemli (Sedimentary cover of the Earth). Moscow: Nauka; 1980. 1–78 p. [35] Kempe S, Degens ET. An early “soda ocean?” Chem. Geol. 1985; 53: 95–108. [36] Kempe S, Kazmierczak J. The role of alkalinity in the evolution of ocean chemistry, organization of living systems and biocalcification processes. In: (Doumenge F, editor. Past and present biomineralization processes: considerations about the carbonate cycle. Monaco: Bull. Inst. Oceanogr. 1994; 13: 61–117. [37] Kempe S, Kazmierczak J. A terrestrial model for an alkaline Martian hydrosphere. Planet. Space Sci. 1997; 45: 1493–9. [38] Schwartzman D. Life, temperature, and Earth. The self-organizing biosphere. New York: Columbia University Press; 1999. 190 p. [39] Kasting JF. Evolution of the Earth’s atmosphere and hydrosphere: Hadean to recent. In: Engel MH, Marko SA, editors. Organic geochemistry: principles & applications. New York and London: Plenum Press; 1993. 611–21 p. [40] Berner RA. GEOCARB II: a revised model of atmospheric CO2 over Phanerozoic time. Am. J. Sci. 1994; 294: 56–91. [41] Ryskov YaG, Demkin VA. Rasvitie pochv i prirodnoi sredy stepey Yuzhnogo Urala v golocene (Development of soils and natural environment during Holocene. Reconstruction based on the geochemistry of stable isotopes). Puschino: ONTI PSC Russian Academy of Sci.; 1997. [42] Retallack GJ. Soils of the past: an introduction to paleopedology. Boston: Unwin-Hyman; 1997. 520 p.

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[43] Polynov BB. Kora vyvetrivania (Weathered rocks). In: Selected works, Moscow: Nauka; 1934. [44] Zavarzin GA. Microbial geochemical calcium cycling. Microbiol. 2002; 71(1): 1–17. [45] Karpeta WP. Bedded cherts in the Rietgat formation, Hartbeesfontain, South Africa: a late Archaean to early Proterozoic magadiitic alkaline playa deposit. South Afr. J. Geol. 1989; 92(1): 29. [46] Tindall BJ. Procaryotic life in the alkaline, saline, athalassic environment. In: Rodriguez-Valera F, editor. Halophilic bacteria. Boca Raton: CRC Press; 1988; 31–67 p. [47] Jones BE, Grant WD, Duckworth AW, Doweson GG. Microbial diversity of soda lakes. Extremophiles 1998; 2: 191–200. [48] Zavarzin GA, Zhilina T, Kevbrin VV. The alkaliphilic microbial community and its functional diversity. Microbiol. 1999; 68(5): 503–21. [49] Zavarzin GA, Zhilina TN. Anaerobic chemotrophic alkaliphiles. In: Seckbach J, editor. Journey to diverse microbial worlds—adaptation to exotic environments. Dordrecht: Kluwer; 2000. 191–208 p. [50] Zavarzin GA. Epicontinental soda lakes as supposed relict biotopes for the formation of terrestrial biota. Microbiologia 1993; 62(5): 789–800. [51] Pusheva MA, Pitryuk AV, Zavarzin GA. Na+ and H+-dependent synthesis of ATP by extremely alkaliphilic anaerobes. Dokladi Academi of Sciences 2000; 374(6): 833–5.

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Perspectives in Astrobiology R.B. Hoover et al. (Eds.) IOS Press, 2005 © 2005 IOS Press. All rights reserved.

Author Index Andrus, V.E. Astafieva, M.M. Bonaccorsi, R. Brambati, A. Burckle, L.H. Çiçek, C. Colloton, P.A. Engel, M.H. Gerasimenko, L. Hoover, R.B. Horneck, G. Kolb, V.M. Macko, S.A. Nemliher, J. Omarov, T.B. Orleansky, V. Paepe, R. Perry, R.S.

25 1, 6 11 11 11 21 76 25 38 v, 43 66 76, 120 25 81 86 38 v, 88, 104 120

Piotrowski, A.M. Rapp, K.J. Rettberg, P. Rozanov, A.Yu. Schidlowski, M. Serozhkin, Yu.G. Shkolnik, E.L. Simakov, M.B. Simakova, Y.S. Steele, A. Tashenov, B.T. Toporski, J. Ushatinskaya, G.T. Van Overloop, E. Zaitseva, L. Zavarzin, G.A. Zhegallo, E.A.

11 76 126 v, 132 146 170 196 175 181 187 86 187 196 88, 104 38 201 196

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