JOURNEY TO DIVERSE MICROBIAL WORLDS

Cellular Origin and Life in Extreme Habitats

Volume 2

Journey to Diverse Microbial Worlds Adaptation to Exotic Environments

Edited by

Joseph Seckbach

SPRINGER-SCIENCE+BUSINESS MEDIA, B.V.

A C L P . Catalogue record for this book is available from the Library of Congress.

ISBN 978-94-010-5850-6 ISBN 978-94-011-4269-4 (eBook) DOI 10.1007/978-94-011-4269-4

Printed on acid-free paper

A l l Rights Reserved © 2000 Springer Science+Business Media Dordrecht Originally published by Kluwer Academic Publishers in 2000 Softcover reprint of the hardcover 1st edition 2000 No part of the material protected by this copyright notice may be reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording or by any information storage and retrieval system, without written permission from the copyright owner.

This book is dedicated to: Professor Lawrence Bogorad (Harvard University), my Ph.D. advisor, colleague and dear friend, with our best wishes of health and happiness.

It is also devoted wholly to my versatile personal cell, to my partner, the family nucleus - Fern, to our organelles, Mesha, A vigail, Raziel, Eliezer and Eliyahu and all their symbiotic partners (Efrat, Amos, Shulamit and Rachelie) and their offspring (Shem, Yarden, Maayan, Hillel and Shmuel).

T ABLE OF CONTENTS

Foreword by James T. Staley IX

Preface by Joseph Seckbach xv Acknowledgements xix

I. General Diversity Chapter I. A Vista into the Diverse Microbial Worlds: An Introduction (J. Seckbach & A. Oren). 3 Chapter 2. The Diversity of Fossil Microorganisms in Archaean-Age Rocks (F. Westall &

M.M. Walsh). 15 Chapter 3. Prokaryotic Diversity (F.A. Rainey & N. Ward-Rainey). 29 Chapter 4. Molecular Biology and Genetic Diversity of Microorganisms (V. Torsvik, F.L. Daae,

R.A. Sandaa & L. 0vreas). 43

II. Introduction to Extremophiles Chapter 5. Bacterial Habitats of Extremophiles (M.T. Madigan). 61 Chapter 6. Anaerobes from Extreme Environments (B. Ollivier, B.K.C. Patel & J.-L. Garcia). 73

Ill. Thermophiles and Acidophiles Chapter 7. Sulfur Metabolism Among Hyperthermophiles (K.M. Noll & S.E. Childers). 93 Chapter 8. Acidophilic Microorganisms (J. Seckbach). 107 Chapter 9. New Acidophilic Thermophiles (R.L. Weiss Bizzoco, N. Banish, M. Lu & S. Saavedra). 117

IV. Psychrophiles and Barophiles Chapter 10. Snow Algae: The Effects of Chemical and Physical Factors on their Life Cycles

and Populations (R.W. Hoham & H.U. Ling). 131 Chapter II. An Oceanographic Perspective on Microbial Life at Low Temperature (J.W. Deming &

A.L. Huston). 147 Chapter 12. Deep-Sea Bacteria (A.A. Yayanos). 161

V. AlkaUphiles Chapter 13. Microbial Diversity and Ecology of Alkaline Environments (B.E. Jones & W.D. Grant). 177 Chapter 14. Anaerobic Chemotropic AlkaJiphiles (G.A. Zavarin & T.N. Zhilina). 191 Chapter 15. Alkaliphilic Cyanobacteria (S. Boussiba, X. Wu & A. Zarka). 209

VI. Halophiles Chapter 16. Life at High Salt Concentrations: Possibilities and Limitations (A. Oren). 227 Chapter 17. New Discovered Halophilic Fungi in the Dead Sea (Israel) (A.S. Buchalo, E. Nevo,

S.P. Wasser & P.A. Volz). 239

VII. Symbioses Chapter 18. Symbioses (Living One inside the Other) (B. Biidel). 255

VIII. Bioluminescence Chapter 19. Luminous Bacteria (M. Haygood & S. Allen). 269

IX. Versatile Microbial Life on the Edge Chapter 20. Diversity of Methanogens (D.L. Valentine & D.R. Boone). 289 Chapter 21. Microbial Life on Petroleum (E.Z. Ron). 303 Chapter 22. Rock Dwelling Fungal Communities: Diversity of Life Styles and Colony Structure

(A.A. Gorbushina & W.E. Krumbein) 317

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Chapter 23. Morphology as a Parameter for Diversity of Bacterial Population (M. Heldal). 335 Chapter 24. Surviving Escherichia coli in Good Shape (A. Zaritsky, C.L. Woldringh,

R.H. Pritchard & I. Fishov). 347

X. Astrobiology and Microbial Candidates for Extraterrestrial Life Chapter 25. Introduction to Astrobiology: Origin, Evolution, Distribution and Destiny of Life in the

Universe (J. Seckbach, F. Westall & J. Chela-Flores). 367 Chapter 26. Life in the Cold and Dry Limits: Earth, Mars and Beyond (Ch.P. McKay). 377 Chapter 27. Terrestrial Microbes as Candidates for Survival on Mars and Europe (J. Chela-Flores). 387

Author Index 399

SubjectIndex 401

Biodata of James T. Staley contributer ofthe Foreword to this volume.

Dr. Jim Staley is currently a Professor of Microbiology at the University of Washington and Vice Chairman of Bergey's Manual Trust. He received his Ph.D. at the University of California, Davis in 1967. Dr. Staley has been interested in bacterial diversity throughout his career. Early on he coined the term 'prostheca' to describe the group of cellular appendages produced by Caulobacter, Prosthecobacter, Hyphomicrobium and the polyprosthecate bacteria such as Stella and Ancalomicrobium. As a microbial autecologist, he has studied microorganisms in freshwater, marine, desert and polar environments. More recently he has been interested in the bacteriology of polar sea ice environments and, based on that work, proposed a set of biogeography and co-evolution postulates to aid in the determination of whether bacteria are cosmopolitan or endemic. Recent work in his lab has shown that strains of the genus Simonsiella, an oral commensal bacterium of mammals, have coevolved with their hosts including humans, sheep, dogs and cats. Dr. Staley has published more than 100 research papers and co-authored a textbook on general microbiology and microbial diversity. E-mail: jtstaley@u.washington.edu

IX

FOREWORD It's the Little Things in Life that Count the Most

Most microbiologists appreciate the remarkable diversity of microbial life. After all, microorganisms were the exclusive inhabitants of Earth for a period of about three billion years (Ga). But even to those familiar with microorganisms, their vast diversity as revealed by the Tree of Life, came as a surprise (Figure I). In contrast, plants and animals evolved only in the past 600 million years. Thus, the "microbial era" persisted for a long interval of time during which speciation and evolution led to much of the diversification of life on Earth.

Perhaps even more important than the duration of the microbial era, however, is the fact that microbial life was here first (Woese, 1998). Many of the resources available to sustain life and allow for early speciation already existed in abundance at the time of Earth's formation. A variety of energy sources including sunlight and reduced inorganic and organic compounds were available before life originated. These included chemical substances such hydrogen gas, sulfide, sulfur, ammonia, reduced iron and hydrocarbons to mention a few. Biological systems evolved to generate energy from these and other reduced substances in the environments, by oxidizing them in the absence of oxygen. Sunlight was also available and evidence for photosynthesis extends back in time to at least three Ga ago. Apart from the success that plants have had in becoming the dominant photosynthetic organisms on land, microorganisms still exclusively utilize most of these early energy sources. Thus, to rephrase an old expression, "The early bugs got the works."

Unlike animals and plants, microbial life is found in every ecosystem on Earth. Where there is life, there is microbial life. Indeed, when major climatic, astronomical and geological events impact Earth, the least affected types of life are microorganisms. In contrast, entire groups of animals, as exemplified by the dinosaurs, can become extinct in a very short period of time.

One of the most fascinating aspects of microbiology, as amply exemplified in this book, is that some microorganisms evolved to live under conditions that are too harsh for animals and plants. Extremes of temperature, pH, oxidation-reduction potentials, salinity and humidity and combinations of these are found in habitats on Earth only colonized by microorganisms. Microbial life is teeming in these unusual habitats and, although macroorganisms are more "advanced" forms of life, they have not successfully replaced the microorganisms.

The Tree of Life, produced in large part through the efforts of Carl Woese (1994), provided the first truly scientific view of biological diversity (Figure I). This is because the Tree of Life is based on sequence comparisons of a macromolecule found in all living organisms, that of the sequence of the RNA from the small subunit of the ribosome. Sequences from some other highly conserved macromolecules such as ATPases and elongation factors produce very similar trees. Each branch in the Tree of Life represents a major phylogenetic group of life. Thus, there is a branch for plants and another for animals that are considered to be Kingdoms. But look at all the remaining branches (i.e., Kingdoms)! In addition to those shown, more than 20 other major branches of microbial life have been detected in environments but as yet, isolated strains

xi

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are not yet available (Hugenholtz et aI., 1999), and it is likely that several more remain to be discovered.

Despite the striking evidence provided by the Tree of Life, some biologists, such as Ernst Mayr (1998) have cast doubt on the biodiversity of microbial life. Mayr states that "Archaebacteria.even where combined with the eubacteria, as prokaryotes, this group does not reach anywhere near the size and diversity of the eukaryotes." Biologists who, like Mayr, base their views of diversity on organismal morphology have difficulty comprehending the vast physiological and metabolic diversity of microorganisms.

Bacteria A,.,luua

Eucarya

Plandomycetft Animals

Vernu:'Ondcrobla Fun"

Red Alg.~

AcellUlar Slime Molds

Figure 1. A diagrammatic representation of the Tree of Life based on 16S and 18S rRNA analyses showing the Bacteria, the Archaea and the Eukarya (modified after Woese et a!., 1990). In addition to the branches shown, many additional microbial phyla exist most of which contain organisms that have not yet been isolated in pure culture.

Perhaps, to make the point more clear, microbiologists should ask such biologists questions like: "Where are the hyperthermophilic animals and plants that live on sulfide as an energy source?" "Why is it that the only carbon dioxide fixation pathway used by plants is the Calvin-Benson cycle which evolved from bacteria? "Do any animals have the ability to live on carbon monoxide and methane as energy sources." "Where do the plants that generate methane gas live?" "Which plants and animals produce sulfuric acid

xiii

and live at pHs as low as I?" "Are there any animals or plants that can carry out photosynthesis or chemosynthesis anaerobically?" These sorts of questions should encourage 'nay sayers' to appreciate the significance that metabolism and physiology have played as driving forces for the evolution and diversification of life.

Then, too, there is the problem of the species definition. Mayr (1998) concludes that microbial diversity is low based on the numbers of extant, described species. He states "Approximately 10,000 eubacteria have been named. The number of species of eukaryotes probably exceeds 30 million; in other words, it is greater by several orders of magnitude." This view is misleading for two very important reasons. First, most bacteria have not yet been named. The vast majority live in ecosystems still awaiting their discovery by a microbiologist. It is estimated that far less than 0.1% of the bacteria have been isolated and described. But an even greater problem with such statements is that they assume that the bacterial species definition is equivalent to the definition of plants and animals.

Two lines of evidence indicate that the bacterial species definition is much broader than that of animals and plants. Based on molecular characteristics such as DNA base composition range, DNA/DNA reassociation values and range of 16S and I8S rDNA sequence, it has been concluded that Escherichia coli, as a species, is defined much more broadly than that of its host mammalian species. Indeed, it is approximately equivalent to the animal Order, several taxonomic ranks above the species (Staley, 1997; Staley, 1999). Likewise, co-divergence of the bacterial genus, Simonsiella with its host animal species, humans, sheep and dogs, indicates that a single species of Simonsiella (Hedlund and Staley, submitted) exists for each animal Order (Primates, Ruminantia, and Carnivora, respectively). Thus, again the bacterial species is approximately equivalent in evolutionary divergence to the animal Order. If co-speciation can be demonstrated at the species level in the animal hosts, then Simonsiella would represent a genus with a single species for each mammalian species. In other words, there would be more than 4,500 species of Simonsiella alone!

Much of the future of biology, and astrobiology, too, lies in microbiology. Many of the great questions of science cannot be answered without understanding microorganisms. "How did life begin?" "What were the first organisms like?" "What were their energy sources and electron acceptors?" "How did the initial speciation events occur?" "How resilient is life?" "Have any bacterial lineages become extinct?" "How did the eukaryotic cell evolve?" "To what extent did gcnes derived from bacteria and their organelles playa role eukaryotic cell evolution?" "What are the minimal genetic and metabolic needs of a free-living organism?"

Using modest resources, microbiologists are just beginning to comprehend the vast unknown diversity of microorganisms in Earth's biosphere. They more fully appreciate the evolutionary implications of animals and plants evolving into a world dominated by microorganisms that have made the existence of all life possible. Increasingly, as microbiologists work in their labs and in the field, it is becoming apparent to all scientists, and even some lay people, that the microbial world and its importance to life on Earth and elsewhere in the Universe, can no longer be denied or ignored.

This book provides an escape from our conventional views of biology. Sit back and read about the remarkable and marvelous world of microbial biodiversity.

xiv

Acknowledgements

I appreciate the helpful comments of Brian Hedlund and Cheryl Jenkins as well as Joseph Seckbach and some anonymous editors.

References

Hedlund, B. P. and Staley, 1. T. Co-speciation of the commensal bacterium Simonsiella with its mammalian hosts. Submitted for publication.

Hugenholtz, P., Goegel, B. M. and Pace, N. R. (1998) 1. Bacteriol. 180: 4765-4774. Mayr, E. (1998) Proc. Nat'!. Acad. Sci. 95: 9720-9723. Staley,1. T. (1997) Current Opinion in Biotech. 8: 340-345. Staley, 1. T. (1999) ASM News 65: 681-687. Woese, C. R. (1994) Microbiol. Rev. 58: 1-9. Woese, e. R. (1998) Proc. Nat'!. Acad. Sci. 95: 11043. Woese, e. R., O. Kandler, and Wheelis, M.e. (1990) Proc. Nat'l. Acad. Sci. USA 87: 4576-4579.

University of Washington Seattle, WAUSA 98195 <Jtstaley@w.washington.edu> 15 February 2000

James T. Staley

Biodata of Joseph Seckbach, editor of this volume, and the chief editor of the book­series of COLE (Cellular Origin and Life in Extreme Habitats). He is the author of the chapters "Acidophilic Microorganisms," "A Vista into the Diverse Microbial World: An Introduction to Microbes at the Edge of Life" (with co-author A. Oren), and "Introduction to Astronomy; Origin, Evolution, Distribution and Destiny of Life in the Universe" (with co-authors F. Westall and J. Chela-Flores) in this current volume.

Dr. Joseph Seckbach edited (and contributed two chapters to) Enigmatic Microorganisms and Life in Extreme Environments (Kluwer Academic Publishers, The Netherlands, 1999). See: http://www.wkap.nl/bookcc.htm/O-7923-S492-3. Likewise, he organized and contributed to the "Cyanidium book" entitled Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells [Kluwer, 1994, see: http://www.wkap.nllbookcc.htm/0-7923-2635-0]. He is the co-author (with author R. Ikan) of the Hebrew-language publication Chemistry Lexicon (1991, 1999) and co-editor of From Symbiosis to Eukaryotism: Endocytobiology VII (E. Wagner et aI., eds.) published by the University of Freiburg and Geneva (1999).

Dr. Seckbach earned his Ph.D. from the University of Chicago (1965) and spent his postdoctoral years in the Division of Biology at Caltech (Pasadena, CA). Then he headed a team at the University of California, Los Angeles (UCLA) searching for extraterrestrial life. Dr. Seckbach has been with the Hebrew University of Jerusalem since 1970 and performed algal research and taught Biological courses. He spent sabbatical periods in Tiibingen (Germany), UCLA and Harvard University. At Louisiana State University (LSU, Baton Rouge), he served (199711998) as the first selected occupant of the John P. Laborde endowed Chair for the Louisiana Sea Grant and Technology Transfer, and as a visiting Professor in the Department of Life Sciences.

Among his publications are books, scientific articles concerning plant ferritin (phytoferritin), cellular ultrastructure, evolution, acido-thermophilic algae, and life in extreme environments. He has also edited and translated books of popular science. Dr. Seckbach's recent interest is in the field of enigmatic microorganisms and life in extreme environments.

E-Mail: seckbach@cc.huji.ac.i1

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.. You. 0 Lord my God, have done many things; the wonders You have devised for us; none can equal You, I would rehearse the tale of them, but they are more than can be told." (Psalms 40, 6)

PREFACE: VOYAGE TO THE EDGES OF LIFE

The purpose of this treatise is to introduce the teacher, researcher, and student as well as the "open minded" reader to some new aspects of uncommon and lesser-known diversity and variability among living microorganisms. Life is ubiquitous on Earth and some of these microorganisms or their products may serve not only for the textbook information but also for applied industrial products. This is the second book in the COLE (Cellular Evolution and Life in Extreme Habitats) series published by Kluwer. This new volume follows the first link entitled Enigmatic Microorganisms and Life in Extreme Environments (1999), see: http://www.wkap.nllbookcc.htm/O-7923-5492-3. In the last two decades interest has grown in the field of microbial life under extreme habitats. [n previous volumes-Enigmatic Microorganism and Evolutionary Pathways and Enigmatic Algae (1994) (see: http://www.wkap.nllbookcc.htm/0-7923-2635-0)-we also dealt with aspects of cellular origins and with habitats where microbes have been detected under very exceptional living conditions.

[n this volume, we take a new voyage to the edges of life. In ten sections, almost thirty researchers present current, updated reviews covering this sphere of knowledge. Our experts in these fields deal with areas from fossilized data and cruise along several lines of extremophiles up to possibilities of extraterrestrial life. This book covers a wide range of extremophiles. There are discussions on hyperthermophiles (Archaean thriving up to 113°C) and Psychrophiles (such as Antarctic cells), microbes which live at the edges of pH ranges (acidity vs. alkalinity) and in hypersaline medium (Prokaryotes and newly discovered Fungi living in 30% salt solution in the Dead Sea, Israel). Other manuscripts deal with additional niches of severe environments; A chapter is devoted to the phenomena of symbiosis in which organisms of different species share one cellular habitat; bioluminescence of bacteria, the diversity of methanogens, rock-dwelling fungi, microbial life on petroleum, and polymorphism in bacteria. Finally, three chapters are devoted to the analogues of harsh terrestrial environments, like Antarctica and Yellowstone hot springs (Wyoming, USA), to the survival of "our" cellular candidates on Mars, Europa (the Juvian moon), and beyond. Our contributors have a wide geographical distribution, coming from the USA, Israel, Germany, Italy, Norway, UK, France, The Netherlands, and Russia.

This timely volume reflects the growing number of people who are involved in these studies and the ever increasing output of books on these subjects. It is our hope that the windows opened in this volume exposing life in various extreme habitats will lead to further discoveries of presently unknown microbial biodiversity occurring at the edge of Life.

Hebrew University of Jerusalem

Seckbach@cc.huji.ac.il March 2000

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Joseph Seckbach

Acknowledgements

I would like to thank our board members, Professors Aharon Oren, Ian Dundas, Russell Chapman and Raphael Ikan for their support and assistance in various steps of "making" this volume. Specific gratitude and appreciation are due to Professor Aharon Oren (Hebrew University) who took an active interest and involvement this volume and in the COLE (Cellular Origin and Life in Extreme Environments) book series. He also proofread several of our manuscripts and always made constructive suggestions and corrections. I thank also Professor Woody Hastings (Harvard University) and Ian Dundas (University of Bergen, Norway) for their critical reviewing of manuscripts. In addition, I express much gratefulness to our contributors and mainly to the "Early Birds" who submitted their chapters in due time and admire their understanding and patience. The publishing team of Kluwer who deal with this book is also acknowledged with appreciation. Last but not least, gratefulness and' gratitude, are due to my wife, Fern Seckbach for assisting in proofreading, suggestions, understanding and much patience during the making ofthis volume.

Hebrew University Jerusalem, Israel seckbach@cc.huji.ac.il March 2000

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Joseph Seckbach