Extremophiles as Astrobiological Models Scrivener Publishing 100 Cummings Center, Suite 541J Beverly MA, 01915-6106 Astrobiology Perspectives on Life of the Universe Series Editors: Richard Gordon and Joseph Seckbach In his 1687 book Principia, Isaac Newton showed how a body launched atop a tall mountain parallel to the ground would circle the Earth. Many of us are old enough to have witnessed the realization of this dream in the launch of Sputnik in 1957. Since then our ability to enter, view and understand the Universe has increased dramatically. A great race is on to discover real extraterrestrial life, and to understand our origins, whether on Earth or elsewhere. We take part of the title for this new series of books from the pioneering thoughts of Svante Arrhenius, who reviewed this quest in his 1909 book The Life of the Universe as Conceived by Man from the Earliest Ages to the Present Time. The volumes in Astrobiology Perspectives on Life of the Universe will each delve into an aspect of this adventure, with chapters by those who are involved in it, as well as careful observers and assessors of our progress. Guest editors are invited from time to time, and all chapters are peer- reviewed. Publishers at Scrivener Martin Scrivener ([email protected]) Phillip Carmical ([email protected]) Scrivener Publishing 100 Cummings Center, Suite 541J Beverly MA, 01915-6106 Astrobiology Perspectives on Life of the Universe Extremophiles as Astrobiological Models Series Editors: Richard Gordon and Joseph Seckbach In his 1687 book Principia, Isaac Newton showed how a body launched atop a tall mountain parallel to the ground would circle the Earth. Many of us are old enough to have witnessed the realization of this dream in the launch of Sputnik in 1957. Since then our ability to enter, view and understand the Universe has increased dramatically. A great race is on to discover real extraterrestrial life, and to understand our origins, whether on Earth or elsewhere. We take part of the title for this new series of books from the pioneering thoughts of Svante Arrhenius, who reviewed this quest in his 1909 book The Life of the Universe as Conceived by Man from the Earliest Ages to the Present Time. The volumes in Astrobiology Perspectives on Life of the Universe will each delve into an aspect of this adventure, with chapters by those who are involved in it, as well as careful observers and assessors of our progress. Guest editors are invited from time to time, and all chapters are peer- reviewed. Publishers at Scrivener Martin Scrivener ([email protected]) Phillip Carmical ([email protected]) Edited by Joseph Seckbach and Helga Stan-Lotter This edition first published 2021 by John Wiley & Sons, Inc., 111 River Street, Hoboken, NJ 07030, USA and Scrivener Publishing LLC, 100 Cummings Center, Suite 541J, Beverly, MA 01915, USA © 2021 Scrivener Publishing LLC For more information about Scrivener publications please visit www.scrivenerpublishing.com. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording, or otherwise, except as permitted by law. Advice on how to obtain permission to reuse material from this title is available at http://www.wiley.com/go/permissions. 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Library of Congress Cataloging-in-Publication Data ISBN 978-1-119-59168-9 Cover image: Courtesy of the editors Cover design and illustrations by Russell Richardson Set in size of 11pt and Minion Pro by Manila Typesetting Company, Makati, Philippines Printed in the USA 10 9 8 7 6 5 4 3 2 1 Contents Preface xiii Part I Extremophiles in Environments on Earth with Similarity to Space Conditions 1 1 Volcanic Steam Vents: Life at Low pH and High Temperature 3 Richard L. Weiss Bizzoco and Scott T. Kelley 1.1 Introduction 3 1.2 Steam Cave and Vent Sites 5 1.3 Steam Cave and Vent Sample Collection 5 1.3.1 Steam Collection 7 1.3.2 Steam Deposit Collection 8 1.3.3 Steam and Steam Deposit Collection: Control Methods 11 1.4 Culture Isolation 13 1.5 Cell Structure of Isolates 16 1.6 Environmental Models 17 1.7 Conclusions 18 Acknowledgments 18 References 19 2 Rio Tinto: An Extreme Acidic Environmental Model of Astrobiological Interest 21 Ricardo Amils and David Fernández-Remolar 2.1 Introduction 21 2.2 Acidic Chemolithotrophy 22 2.3 Rio Tinto Basin 24 2.4 Biodiversity in the Tinto Basin 25 2.5 Tinto Basin Sedimentary Geomicrobiology 27 2.6 The Iberian Pyrite Belt Dark Biosphere 29 2.7 Methanogenesis in Non-Methanogenic Conditions 34 2.8 Rio Tinto: A Geochemical and Mineralogical Terrestrial Analog of Mars 35 2.9 Conclusions 37 References 38 3 Blossoms of Rot: Microbial Life in Saline Organic-Rich Sediments 45 Adrian-Ștefan Andrei, Paul-Adrian Bulzu and Horia Leonard Banciu 3.1 Introduction 46 3.2 Overview of Saline Aquatic Systems 47 v vi Contents 3.3 Prerequisites of Organic Carbon-Rich Sediment Genesis in Saline Lakes 48 3.4 Chemistry of Recent Organic Carbon-Rich Sediments in Saline Water Bodies 48 3.5 Microbial Life in Saline Sapropels 49 3.5.1 Higher-Order Microbial Taxonomy Detected in Modern Saline Sapropels 53 3.5.2 Anaerobic Organic Matter Degradation in Saline Organic Carbon-Rich Sediments 54 3.5.2.1 Hydrolysis of Biomacromolecules 54 3.5.2.2 Primary and Secondary Fermentation of Low Molecular Weight Molecules 57 3.5.2.3 Methanogenesis 58 3.5.2.4 Biological Sulfur Reduction and Oxidation 60 3.5.2.5 Nitrogen Cycling 62 3.5.3 Uncultured Microbial Diversity of Saline Sapropels and Its Putative Ecological Roles 62 3.5.3.1 Uncultured Bacteria 63 3.5.3.2 Uncultured Archaea 64 3.6 Relevance of Saline Sapropels 65 3.7 Concluding Remarks 65 Acknowledgments 66 References 66 4 The Haloarchaea of Great Salt Lake as Models for Potential Extant Life on Mars 83 Madelyn Bayles, Bradley C. Belasco, Alexander J. Breda, Calli B. Cahill, Adrik Z. Da Silva, Michael J. Regan Jr., Nicklaus K. Schlamp, Mariah P. Slagle and Bonnie K. Baxter 4.1 The Great Salt Lake System in the Bonneville Basin 84 4.1.1 A Significant Terminal Lake in North America 84 4.1.2 Great Salt Lake as an Extreme Environment 84 4.1.3 The Declining Elevation of Great Salt Lake 87 4.1.4 Pertinent Mineralogy of Great Salt Lake and the Bonneville Basin 88 4.2 The Transformation of an Ancient Wet Mars to a Modern Hostile Environment 89 4.2.1 Global Climatic Change on Mars 90 4.2.2 The Ancient Lacustrine Environments of Mars 91 4.2.3 Brine on the Martian Surface 93 4.2.4 Mars is a Hostile Environment for Life 94 4.3 Life in Evaporitic Minerals on Earth 95 4.3.1 Formation of Halite and Gypsum Primary Crystals in Aquatic Environments 95 4.3.2 Haloarchaea May Be Entombed in Halite 96 4.3.3 Haloarchaea May Be Entombed in Gypsum 96 Contents vii 4.3.4 Haloarchaea Can Survive over Geologic Time in Fluid Inclusions 97 4.4 Great Salt Lake Haloarchaea 97 4.5 Haloarchaea Have Superpowers for Extreme Lifestyles 99 4.5.1 Haloarchaea May Show Versatility with Respect to Temperature and pH 99 4.5.2 Haloarchaea are Metabolically Versatile 101 4.5.3 Haloarchaea Are Adapted to High Salinity and Desiccating Conditions 101 4.5.4 Haloarchaea Are Resistant to Ultraviolet Radiation 102 4.5.5 Haloarchaea Are Resistant to Ionizing Radiation 103 4.5.6 Haloarchaea May Have Novel Nutrient Attainment Strategies for Dormancy Periods 104 4.5.7 Haloarchaea Are Resistant to Space Conditions 104 4.6 Extant or Extinct Haloarchaea on Mars? 105 4.6.1 Haloarchaea as Extant Life 105 4.6.2 Haloarchaea as Extinct Life 106 4.7 Conclusions and Insights 108 Acknowledgments 109 References 109 5 Arsenic-and Light Hydrocarbon-Rich Hypersaline Soda Lakes and Their Resident Microbes as Possible Models for Extraterrestrial Biomes 125 Ronald S. Oremland 5.1 Introduction 125 5.2 Mars 129 5.3 Enceladus 131 5.4 Titan 132 References 134 6 Antarctic Bacteria as Astrobiological Models 137 Carmel Abbott and David A. Pearce Abbreviations 137 6.1 Introduction 138 6.2 Antarctica as an Analogous Environment for Astrobiology 139 6.2.1 Temperature 140 6.2.2 Soil as a Life-Supporting Medium 140 6.2.3 Soil Salinity 142 6.3 Astrobiological Environments of Interest 142 6.4 Bacterial Adaptations to Extreme Environments as Analogues for Astrobiology 143 6.4.1 Psychrophiles 144 6.5 Antarctic Bacteria as Analogues for Astrobiology 145 6.6 Endemic Antarctic Bacteria used in Astrobiology 146 6.7 Cosmopolitan Bacteria Found in Antarctica and used in Astrobiology 151 viii Contents 6.8 Conclusion 152 References 153 7 Extremophilic Life in Our Oceans as Models for Astrobiology 161 Robert Y. George 7.1 Introduction 162 7.2 Southern Ocean Ecosystem: West Antarctic Peninsula Region 162 7.3 Sea Ice Decline in WAP and Ice Shelf Collapse in Amundsen Sea 162 7.4 Deoxygenation Leading toward Hypoxic Zone in Amundsen Sea 164 7.5 Microbial Extremophiles in Southern Ocean 165 7.6 Chemosynthetic Abyssal Ecosystems 166 7.6.1 Methane Cold Seep Deep-Sea Communities in the Abyss 166 7.6.2 Are Hydrothermal Vents Abyssal Gold Mines? 167 7.7 Hydrothermal Activity in Hrad Vallis on Mars 170 7.8 Why Chemosynthetic Ecosystems Remind Us of Environmental Conditions When Life Originated in the Universe 172 7.9 Ultra-Abyssal Ecosystem: Puerto Rico Trench 173 7.10 Affiliations of Abyssal Life to Astrobiology: Some Perspectives 175 7.11 Can We Find Protozoans Such as Xenophyophores on Other Planets? 177 7.12 Barophilic Organisms in the Deep-Sea 178 Acknowledgments 179 References 180 Part II Extremophiles in Space (International Space Station, Others) and Simulated Space Environments 183 8 Challenging the Survival Thresholds of a Desert Cyanobacterium under Laboratory Simulated and Space Conditions 185 Daniela Billi 8.1 Introduction 185 8.2 Endurance of Chroococcidiopsis Under Air-Drying and Space Vacuum 186 8.3 Endurance of Chroococcidiopsis Under Laboratory Simulated and Space Radiation 189 8.4 The Use of Chroococcidiopsis’s Survival Thresholds for Future Astrobiological Experiments 191 Acknowledgments 192 References 192 9 Lichens as Astrobiological Models: Experiments to Fathom the Limits of Life in Extraterrestrial Environments 197 Rosa de la Torre Noetzel and Leopoldo García Sancho 9.1 Introduction 197 9.2 Survival of Lichens in Outer Space 199 9.3 Space Environment: Relevance in Space Science 200 9.3.1 Space Radiation 200 9.3.2 Temperature 201 9.3.3 Microgravity 201 Contents ix 9.4 Biological Effects of Space 201 9.4.1 Extraterrestrial Solar UV Radiation 201 9.4.2 Cosmic Radiation 202 9.4.3 Space Vacuum 202 9.4.4 Microgravity 203 9.5 Current and Past Astrobiological Facilities for Experiments with Lichens 203 9.6 Space Experiments with Lichens 206 9.6.1 The BIOPAN Experiments: Exposure to Outer Space Conditions 206 9.6.2 EXPOSE Facility On Board the ISS: Experiments at Space- and Mars-Like Conditions 211 9.7 Simulation Studies 214 9.8 Summary and Conclusions 215 9.9 Future Possibilities and Recommendations 216 References 216 10 Resistance of the Archaeon Halococcus morrhuae and the Biofilm-Forming Bacterium Halomonas muralis to Exposure to Low Earth Orbit for 534 Days 221 Stefan Leuko, Helga Stan-Lotter, Greta Lamers, Sebastian Sjöström, Elke Rabbow, Andre Parpart and Petra Rettberg 10.1 Introduction 222 10.2 Material and Methods 223 10.2.1 Cultivation 223 10.2.2 UV-C Radiation and Desiccation Resistance 223 10.2.3 Sample Preparation for Exposure 223 10.2.4 Pre-flight Ground Tests 224 10.2.5 Flight Preparation and Mission Ground Reference (MGR) Preparation 224 10.2.6 Mission EXPOSE-R2 – Flight Parameters and Conditions 225 10.2.7 Survival 226 10.2.8 Stability of Genomic DNA 227 10.2.9 Integrity of 16S rRNA Gene 227 10.3 Results 228 10.3.1 Survival EVT/SVT 228 10.3.2 Survival and Genetic Integrity Following Space Flight 228 10.4 Discussion 232 Acknowledgments 233 References 233 11 The Amazing Journey of Cryomyces antarcticus from Antarctica to Space 237 Silvano Onofri, Claudia Pacelli, Laura Selbmann and Laura Zucconi 11.1 Introduction 238 11.2 The McMurdo Dry Valleys 238 11.3 Cryptoendolithic Communities 239 11.4 The Black Microcolonial Yeast-like Fungus Cryomyces antarcticus 240 11.5 The Polyextremotolerance of Cryomyces antarcticus 240