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ENIGMATIC MICROORGANISMS AND LIFE IN EXTREME ENVIRONMENTS
Cellular Origin and Life in Extreme Habitats
Volume 1
Enigmatic Microorganisms and Life in Extreme Environments
Edited by
J oseph Seckbach
SPRINGER SCIENCE+BUSINESS MEDIA, B.V.
A C.I.P. Catalogue record for this book is available from the Library of Congress.
Enigmatic microorganisms and life tn extre.e envtron.ents I edtted by Joseph Seckbach.
p. c •. -- (Cellular ortgtn and ltfe tn extreme habttats ; v. 1>
Includes tndex.
ISBN 978-1-4020-1863-3 ISBN 978-94-011-4838-2 (eBook) DOI 10.1007/978-94-011-4838-2
1. Extreme environments--Mtcrobtology. I. Seckbach, J. (Joseph) II. Sertes. OR100.9.E54 1998 579' . 17--dc21
ISBN 978-1-4020-1863-3
Printed on acid-free paper
AII Rights Reserved © 1999 Springer Science+ Business Media Dordrecht
Originally published by Kluwer Academic Publishers in 1999 Softcover reprint ofthe hardcover lst edition 1999
98-48551
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: Fern Seckbach, a critique, proofreader, colleague, friend, catalyst and .... wife.
T ABLE OF CONTENTS
Foreword by Russell L. Chapman 0000000000000 0 0 0 000 0 0 0 0 0 0 0 0 0 0 0 0 0 0 000 0 0 xiii
Preface by Joseph Seckbach 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 xvii
Acknowledgement 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 xxi
I. In the Beginning: Origin and Evolution of the First Cells ................. 1
Chapter I: Tracing the Relationships among the Eubacteria using cr70_ Type Sigma Factors o. 3
Tanja Mo Gruber and Donald Ao Bryant
Chapter 2: Gene Transfer in Early Evolution 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 15
Lorraine Olendzenski and Jo Peter Gogarten
Chapter 3: The Evolution of Algae 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 29
AoWoDo Larkum
Chapter 4: From Bacteria to Protista 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 49
Hakobu Nakamura
Chapter 5: Eukaryogenesis: The Search/or an Evolutionary Transition towards Intelligence in an Extreme Environmental Habitat a/the Outer Solar System 000000 0 0 0 0 0 0 0 63 - Julian Chela-Flores
Chapter 6: Fossil Bacteria 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 73 - Frances Westall
Chapter 7: Growth and Organisms in Ammonia: Kakabekia, a Microbial Enigma 0 0 0 0 0 0 0 0 0 89 - BoZo Siegel
viii
II. Enigmatic Microorganisms •....................................... 97
Chapter 8: Enigmatic Unicellular Protista: Are They Really Enigmatic? The Algae Case ... 99
David J. Chapman
Chapter 9: The Prochlorophytes - An Algal Enigma. Biology of Chlorophyll alb Containing Photosynthetic Prokaryotes ................................ 113
A.F. Post
Chapter 10: Cryptomonad Systemastics - An Algal Enigma? ......................... 127
Paul Kugrens
Chapter 11: The Organellar Genomes of Cyanidioschyzon merolae .................... 139
Niji Ohta, Naoki Sato and Tsuneyoshi Kuroiwa
III. The Versatile Extension of Life .................................... 151
Chapter 12: The Versatility of Microorganisms .................................... 153
Maud M. Walsh and Joseph Seckbach
Chapter 13: Eukaryotic Cells under Extreme Conditions ............................. 163
D.McL. Roberts
Chapter 14: The Poikilotrophic Micro-Organism and its Environment. Microbial Strategies of Establishment, Growth and Survival ................................ 175
A.A. Gorbushina and W.E. Krumbein
Chapter 15: The Study of Enigmatic Microbial Communities ......................... 187
T.E. Jensen and W.A. Corpe
Chapter 16: Nanobacteria and Man ............................................. 195
E. Olavi Kajander, Mikael Bjorklund and Neva <;:iftyioglu
Chapter 17: An Enigma in Marine Nanoplankton. The Role of Star-Like Structures Produced by Phaeocystis .................................................... 205
M.-J. Chretiennot-Dinet
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Chapter 18: Algal Versatility in Various Extreme Environments ...................... 215
Josef Elster
IV. Microorganisms in Extreme Environments ..........•............... 229
Dryness
Chapter 19: Enigmatic Desert Soil Algae. Soil Algal Flora of the Western US.A. and Baja California, Mexico ............................................ 231
V.R. Flechtner
Chapter 20: Life in the Rocks - Endolithic Algae .................................. 243 - N. Van Thielen and D.J. Garbary
Chapter 21: Lithobionts in the Eastern Mediterranean ............................... 255
lGarty
Temperature Effects
i. Thermophiles
Chapter 22: Fine Structure of Hyperthermophilic Prokaryotes ........................ 277
R. Rachel
Chapter 23: The Phylogeny of Thermophiles and Hyperthermophiles and the Three Domains of Life. The Phylogeny ofThermophiles ........................ 291
Debashish Bhattacharya, Thomas Friedl and Heiko Schmidt
Chapter 24: Life in the Extreme: New Prokaryotes Living in High Temperature Low pH Environments .................................................... 305
R.L. Weiss Bizzoco
ii. Psychrophiles
Chapter 25: Psychrophilic Yeasts ............................................... 315
H.S. Vishniac
x
Chapter 26: Antarctic Microfungi .............................................. 323
Silvano Onofri
Halophiles
Chapter 27: The Enigma of Square and Triangular Halophilic Archaea ................. 337
A. Oren
Chapter 28: Microbial Life in the Dead Sea ....................................... 357
A. Ventosa and D.R. Arahal
Chapter 29: Salt Sensitivity of Cells ............................................ 369
Hakobu Nakamura
Chapter 30: Survival of Halophilic Bacteria in Ancient Salts: Possibilities and Potentials ... 387
Russell H. Vreeland and William D. Rosenzweig
Chapter 31: Dunaliella p-Carotene. From Science to Commerce ...................... 399
Ami Ben-Amotz
Chapter 32: Haloarchaeal Growth Physiology ..................................... 411
Richard F. Shand and Abril M. Perez
Living in Enormous pH Ranges
i. Acidophiles
Chapter 33: The Cyanidiophyceae: Hot Spring Acidophilic Algae ..................... 425
Joseph Seckbach
Chapter 34: Revision of Comparative Traits for the Acido- and Thermophilic Red Algae Cyanidium and Galdieria ........................................... 437
Wolfgang Gross
Chapter 35: Mechanism and Evolution of Organelle Division ........................ 447
R. Itoh and T. Kuroiwa
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Chapter 36: Dunaliella Acidophila - A Most Extreme Acidophilic Alga ................ 465
Uri Pick
ii. Alkalophiles
Chapter 37: Alkaliphilic Microorganisms ........................................ 479
Masahiro Kamekura
Barophiles
Chapter 38: A Global Perspective on the Microbial Abundance and Activity in the Deep Subsurface ...................................................... 487
T.C. Onstott, T.J. Phelps, T. Kieft, F.S. Colwell, D.L. Balkwill, J.K. Fredrickson and F.J. Brockman
Chapter 39: Membrane-Based Adaptions of Deep-Sea Piezophiles .................... 501
D.H. Bartlett and K.A. Bidle
Chapter 40: Chemoautotrophic Bacteria - Marine Invertebrate Symbioses. Adaptions for Autotrophic Carbon and Nitrogen Assimilation .......................... 513
R.W. Lee
V. Effect of Substances, Gases and Irradiatons ......................... 525
Chapter 41: Growth of Extremophiles on Petroleum ................................ 527
J.M. Foght and D.M. McFarlane
Chapter 42: MetaUogenium - A Microbial Enigma ................................. 539
D. Klaveness
Chapter 43: Microbes and Radiation ............................................ 549
L.J. Rothschild
Chapter 44: The Unknown Life of Airborne Algae ................................. 563
W. Reisser
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VI. Living Together: Symbiosis ....................................... 573
Chapter 45: Organisms Living inside Others. The Symbiotic Wonders .................. 575
Douglas P. Zook
Chapter 46: Symbiogenesis of Bacteria within Amoebae. Symbiogenesis in Amoebae ...... 585
K.W. Jeon
Chapter 47: Symbiotic Associations between Metanogenic Archaea, Protists and Metazoa: Evolutionary Implications ................................ . . . . . . . . . .. 599
lH.P. Hackstein, AH.AM. van Hoek, W.W. Sprenger and l Rosenberg
Chapter 48: Cyanobacteria in Symbioses with Plants and Fungi ....................... 613
B. Bergman, K. Bateman and U. Rasmussen
Chapter 49: The Hard Life of Prokaryotes in the Leaf Cavities of Azolla ................ 629
M. Grilli Caiola and C. Forni
Chapter 50: Freshwater Algal Symbioses in Protoza and Invertebrates . . . . . . . . . . . . . . . . . . 641
V.A.R. Huss
Chapter 51: Intracellular Symbiotic Bacteria within Insects .......................... 651
H. Charles and P. Nardon
Chapter 52: The Mysterious Interrelationships between Fungi and Plants: The Case of Endosymbionts ................................................... 661
James F. White, Jr., Ponaka V. Reddy, Charles W. Bacon and Daniel Cabral
VII. Index ........................................................ 671
Biodata of Russell L. Chapman contributor of the 'Foreword for this volume.
Dr. Russ L. Chapman is Professor of Biological Sciences and the Executive Director of the Center for Coastal, Energy, and Environmental Resources (CCEER), and also an Adjunct Professor in the Department of Oceanography and Coastal Sciences at the Louisiana State University (Baton Rouge, Louisiana). He earned his Ph.D. in 1973 at the University of California, Davis (major: Botany [Phycology]). Dr. Chapman's main research interests are: algal ultrastructure and phylogeny, biology of the Trentepohliaceae (Chlorophyta), ribosomal gene sequencing and molecular evolution in algae and bryophytes. He has been affiliated with several national and international professional committees and societies and is a member of various Honor Societies. As a requested speaker and organizer, he has delivered many invited lectures and symposia presentations and has been a member of invited workshops, and consulting and review teams (nationally and internationally). E-Mail: [email protected]
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Foreword
Modern methods and approaches, such as the analysis of molecular sequences to infer evolutionary relationships among organisms, have provided vast new sets of data to further our understanding ofliving organisms, but there remain enigmas in the biological world that will keep scientists working and thinking for decades. Microorganisms by virtue of their small size and almost unbounded diversity provide ample examples of intriguing mysteries that are being challenged with all of the techniques the modern scientific arsenal can provide. One whole arena of this battle to resolve puzzling mysteries about various microorganisms is the almost unbelievable ability of many micro-organisms to live in extreme environments. Whether the challenge is extreme heat, cold, pressure, hypersalinity, alkalinity or acidity, some micro-organisms live now where no life might seem possible. This fascinating state of affairs is the context for this present volume edited by Joseph Seckbach.
This Volume is a compilation of many of the especially interesting questions and biological challenges that arise in the consideration of microorganisms in general and the extremophiles in particular. Although the editor has his own special interest in Cyanidium caldarium and will never miss the chance to share information about this particular intriguing alga (and its cohorts), he has brought together the work of many specialists and has covered over a dozen special topics ranging from the origins and evolution ofthe first cells to the varied array of extreme environments in which some microorganisms survive and thrive. Even the special challenges of symbiotic environments and the sometimes controversial topic of exobiology receive attention within the chapters of this book. Whether regarded as a complete review of major topics in our understanding of microorganisms in extreme environments or as a source of detailed coverage of specific topics of particular interest, this book serves as a wonderful source of current information on a wide array of topics on a broad spectrum of organisms. To those who are completely new to the field and to those who seek more information about microorganisms that have already caught their attention, this volume provides a wealth of information as well as a fair measure of mystery and enigma.
Louisiana State University Baton Rouge, LA 14 May 1998
Russell L. Chapman
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Biodata of Joseph Seckbach, editor of this volume, and author of "The Cyanidiaceae: Hot Spring Acidophilic Algae" and coauthor (with M.M Walsh) of " The Versatility of Microorganisms. "
Dr. Joseph Seckbach, served as the first selected occupant (1997/1998) of the John P. Laborde Endowed Chair for Louisiana Sea Grant Research and Technology Transfer, and as visiting Professor in the Department of Life Sciences at Louisiana State University (LSU), Baton Rouge, LA. He earned his Ph.D. from the University of Chicago (Chicago, IL) in 1965, and spent his postdoctoral years in the Division of Biology at Caltech (Pasadena, CA). Then he headed at the University of . Californian at Los Angeles (UCLA) a team for searching of extraterrestrial Life. Dr. Seckbach has been appointed to the faculty of the Hebrew University (in Organic Chemistry and later in the School for Over Seas Students) performing algal research and t~aching (resp.). He spent his sabbatical periods in Tubingen (Germany), UCLA (Los Angeles), and Harvard University (Cambridge, MA). Among his pUblications are three books and numerous scientific articles concerning plant ferritin, Cellular evolution, and acido-thermophilic algae. His recent interest is in the field of enigmatic microorganisms and Life in extreme environments. E-Mail: [email protected]
xvii
"0 Lord, how manifold are your works! in wisdom have you made them all: the Earth is full of your
riches. " Psalms 104, 24
PREFACE
The purpose of this treatise is to introduce the researcher, teacher or student as well as the open-minded reader to some of the variability of living microorganisms and life forms, as we do not always know them. In this volume a few dozen authors review their investigations into enigmatic organisms and life in mysterious habitats.
Life is ubiquitous on Earth and some Extremophiles or their products can find their way into biotechnological research and eventually into industry (e.g., extremozymes). Furthermore, the diversity of life under those extreme environments may serve as a model for the possibilities of life on other celestial habitats (e.g., on Mars, or Europa, the moon of Jupiter).
This volume, one link in the new book series being published by Kluwer Academic Publishers (The Netherlands) is entitled Cellular Origin and Life in Extreme Habitats. This current book follows and supplements the first treatise on the Evolutionary Pathways and Enigmatic Algae (Ed. By J. Seckbach, published by Kluwer, 1994).
The term "enigmatic microorganisms" is a relative concept and refers to life forms that are seen, from the anthropocentric point of view, to be puzzling exceptional creatures. The six sections of this book, containing contributions by over fifty researchers, cover various aspects of these unique mysterious organisms and their environments. The question as whether the Endosymbiosis is the only path for Eukaryogenesis (the evolvement of the bacterium into the first eukaryotic cell) is being addressed by some of our authors in the book's opening section on Origin and Evolution of the First Cells. The chapters on fossilized bacteria and Kakabekia provide additional data on earlier/past microorganisms. Other chapters, in sections Enigmatic Microorganisms and Versatile Extension of Life describe new microbial communities, such as the relatively recently discovered Prochlorophytes, the picoplankton, Cryptomonads, and nanobacteria (also with a relation to man). A similar profile is taken for the extremophilic organisms which colonize bizarre areas of natural uncommon or extreme habitats. A few of our authors present overviews on the general concept of these phenomena and some of them have pointed out that while such environments surely kill the majority of communities, other find it an Elysium.
The Extremophiles can be found at high temperature ranges, for example, the hot springs acidophilic algae (Cyanidiaceae) grow at 45-56°C, while the hyperthermophilic archaea tolerate a temperature range over boiling point (> 100°C). Other organisms discussed live in cold polar zones, such as the psychrophiles or the Antarctic microbes. We present aspects of microbes living at higher levels of pH, interestingly it has been pointed out here that the insect, rose chafer larvae host microbial community at extreme alkaline pH (> 11). While the microorganisms at the hindgut of these insect's larvae live at neutral pH. On the other scale of pH, there are the acidophilic archaea (e.g., Thermoplasma acidophilum), or the eukaryotic unicellular alga Cyanidium caldarium (Cyanidiaceae) and Dunaliella (Chlorophyta) thriving in very acidic habitats (pH ranges 0 - 4.0). Microbial communities have been
xix
xx
isolated from hyper saline areas, lakes or salt mines (containing concentrated salt solutions as exit in the Dead Sea in Israel). Such hyperhalophiles may exhibit unusual cell morphologies (and appear as triangular or square archaean cells, see in the section of Halophiles in this volume). The investigations with the barophilic cells (tolerating pressure of above 600 atmospheres) are presented in three chapters.
Microorganisms are ubiquitous, they have been observed as airborne cells, (e.g., algae), in guts of higher animals and of insects as well as in very dry habitats. Dry desert environments with their low moisture content and exposure to high levels of UV radiation are considered extreme habitats. Most interesting are the microorganisms associated with metals, growing on petroleum, under various gases such as ammonium or under CO2.
Several authors covered the field of Living Together: Symbiosis where two or more organisms of different species share a single habitat or live as symbionts inside the host. Those partners have developed mutual relationships and have continuous cross "talks" between host-symbionts physiological and behavioral interactions. These relationships are long lasting associations between organisms of different species. For example, termites are known to posses symbiotic protists and bacteria in their intestine. Many cockroach species host ciliates and a few have also flagellates in their hind guts. Symbiotic microbial communities are present in digestive tracts of animals consist of anaerobic bacteria, methanogenic archaea, protists, and anaerobic fungi. Thus the animal (or insects) guts are open ecosystems and these microbes degrade plant polymers that are resistant to host digestive enzymes. Methane emission from animal and insects is due to their methanogenic archae a and bacteria. It has been shown that some of these insects' symbionts can inactivate and detoxificate poisonous diets consume by their hosts. In a bovine rumen there are more than 100 different species of symbiotic bacteria (1011 cells per ml rumen fluid) and 50 species of ciliates as well as two-three anaerobic fungi (see the chapter by Hackstein et al. in this volume). Further chapters describe more aspects of the symbiotic phenomena, like the association of cyanobacteria-plants and associations of bacteria-amoeba, algae-protists and invertebrates, bacteria-insects and of fungi-grasses.
This volume's appearance is quite timely as interest in the topic of extremophiles, based on the numbers of people involved in their study, is growing at an everincreasing rate. Twenty years ago there appeared Microbial Life in Extreme Environments (ed. by D.J. Kushner, Academic Press, 1978). More recent works devoted to the topic are Extremophile Mikroorganismen in Ausgefallenen Lebensraumen (ed. by K. Hausmann and B.P. Kremer, VCH publisher, 1995) and Extremophiles: Microbial Life in Extreme Environments (ed. by K. Horikoshi and W.D. Grant, Willy-Liss Publisher, 1998). Our current book complements them.
Hebrew University of Jerusalem Mount Scopus 91905 Israel <[email protected]> August 10, 1998
Joseph Seckbach
Acknowledgements
I would like to acknowledge, in compiling this volume, the assistance of my colleagues at Louisiana State University (LSU) at Baton Rouge, LA. (while I served there as the first selected occupant of The John P. Laborde Endowed Chair for Louisiana Sea Grant Research and Technology Transfer, and as visiting Professor in the Department of Life Sciences at LSU). I thank my generous host, Dr. Jack R. Van Lopik (Executive Director of Sea Grant at the LSU) for his warm hospitality. The efficient technical contributions of Mrs. Brenda Henning (Sea Grant, LS u.) is very much appreciated. Many thanks are due to Dr. Russell Chapman (Executive Director of CCEER at the LSU) and to his devoted team in Biological Sciences for providing a suitable atmosphere and for their kind technical services and hospitality during the final organization and compilation of this book. Personal gratitude and thanks are due to Fern Seckbach, Dr. Maud M. Walsh and to Dr. Aharon Oren for their critical reading some of these manuscripts. Last but not least, I acknowledge the warm cooperation of Rene Mijs (Kluwer Publication) as well as many thanks to all the authors for their contributions and patience.
Hebrew University of Jerusalem Mount Scopus 91905 Israel <[email protected]> August 10, 1998
xxi
Joseph Seckbach
