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HALOPHILIC MICROORGANISMS and THEIR ENVIRONMENTS Cellular Origin and Life in Extreme Habitats HALOPHILIC MICROORGANISMS AND THEIR ENVIRONMENTS Cellular Origin and Life in Extreme Habitats Volume 5 Series Editor: Joseph Seckbach Hebrew University of Jerusalem, Israel Halophilic Microorganisms and their Environments by Aharon Oren The Institute of Life Science, The Hebrew University of Jerusalem, Jerusalem, Israel KLUWER ACADEMIC PUBLISHERS NEW YORK, BOSTON, DORDRECHT, LONDON, MOSCOW eBook ISBN: 0-306-48053-0 Print ISBN: 1-4020-0829-5 ©2003 Kluwer Academic Publishers New York, Boston, Dordrecht, London, Moscow Print ©2002 Kluwer Academic Publishers Dordrecht All rights reserved No part of this eBook may be reproduced or transmitted in any form or by any means, electronic, mechanical, recording, or otherwise, without written consent from the Publisher Created in the United States of America Visit Kluwer Online at: http://kluweronline.com and Kluwer's eBookstore at: http://ebooks.kluweronline.com DEDICATION This book is dedicated to the memory of Donn J. Kushner, one of the founding fathers of halophile microbiology, who passed away on September 15, 2001, at the age of 74. My first meeting with Donn took place at the 1983 ASM meeting in New Orleans. At the time I was a newcomer in the field of halophile science, and I clearly remember how thrilled I was to meet one of the 'big' names in the field. It quickly appeared that we shared not only an interest in science, but in music as well. Donn was an accomplished player of the violin and the viola. We have since performed chamber music together at scientific meetings in Jerusalem (1987), in Alicante (1989, together with Morris Kates playing the violin and Masamichi Kohiyama on 'cello), in Williamsburg (1992, again with Morris Kates' violin and Larry Hochstein's clarinet), and once more in Jerusalem (1997, again joined by Larry Hochstein). I will always remember these informal concerts with colleague halophile scientists as highlights in my career. I hope that the following pages will form a fitting tribute to Donn’s many contributions to our understanding of halophilic microorganisms. Aharon Oren v TABLE OF CONTENTS DEDICATION v TABLE OF CONTENTS vii FOREWORD BY JOSEPH SECKBACH xiii PREFACE xv COMMENTS ON PROKARYOTE NOMENCLATURE AND xix SALT CONCENTRATION UNITS SECTION 1. AN HISTORICAL SURVEY 1 CHAPTER 1. HALOPHILIC MICROORGANISMS IN THEIR NATURAL ENVIRONMENT 3 AND IN CULTURE -AN HISTORICAL INTRODUCTION 1.1. Red brines - early observations and explanations 3 1.2. The first records of the isolation of halophilic 5 Archaea and Bacteria 1.3. Dunaliella and other halophilic algae 8 1.4. Ecological studies: the Great Salt Lake 9 1.5. Alkaline soda lakes 10 1.6. The Dead Sea 11 1.7. The study of biogeochemical processes in hypersaline environments 11 1.8. The beginning of the modern era of halophile research 13 1.9. References 14 SECTION 2.HALOPHILIC MICROORGANISMS AND THEIR PROPERTIES 19 INTRODUCTION 21 CHAPTER 2. TAXONOMY OF HALOPHILIC MICROORGANISMS: ARCHAEA, 23 BACTERIA AND EUCARYA 2.1. The place of halophiles within the microbial world 23 2.2. The halophilic Archaea 25 2.3. The halophilic and halotolerant Bacteria 36 2.4. The halophilic and halotolerant Eucarya 56 2.5. References 57 vii viii CHAPTER 3. THE CELLULAR STRUCTURE OF HALOPHILIC 69 MICROORGANISMS 3.1. Cellular structures of halophilic Archaea 69 3.2. Cellular structures of halophilic Bacteria 99 3.3. Cellular structrues of halophilic Eucarya 110 3.4. References 111 CHAPTER 4. CELLULAR METABOLISM AND PHYSIOLOGY OF HALOPHILIC 125 MICROORGANISMS 4.1. Physiology of halophilic Archaea 125 4.2. Physiology of halophilic Bacteria 146 4.3. Physiology of halophilic Eucarya 152 4.4. Metabolic diversity among the halophiles: a bioenergetic approach 153 4.5. References 157 CHAPTER 5. PIGMENTS OF HALOPHILIC MICROORGANISMS 173 5.1. Algal carotenoids 174 5.2. Pigments of oxygenic and anoxygenic photosynthetic Bacteria 178 5.3. Carotenoids of aerobic heterotrophic Archaea and Bacteria 179 5.4. The retinal pigments: bacteriorhodopsin, halorhodopsin, and sensory rhodopsins 183 5.5. The photoactive yellow protein of Halorhodospira and other halophilic purple bacteria 196 5.6. References 198 CHAPTER 6. INTRACELLULAR SALT CONCENTRATIONS AND ION METABOLISM 207 IN HALOPHILIC MICROORGANISMS 6.1. Introduction 207 6.2. Methods used to estimate intracellular ionic concentrations in halophilic microorganisms 208 6.3. Ion metabolism in the Halobacteriaceae 210 6.4. Ion metabolism in aerobic halophilic Bacteria 214 6.5. Ion metabolism in the Halanaerobiales 223 6.6. Ion metabolism in Dunaliella 223 6.7. References 227 CHAPTER 7. PROPERTIES OF HALOPHILIC PROTEINS 233 7.1. Introduction 233 7.2. Halophilic behavior of enzymes from halophilic Archaea 235 7.3. Purification of halophilic proteins 240 7.4. Salt relationships of selected proteins from halophilic Archaea 249 ix 7.5. Halophilic behavior of enzymes from the aerobic halophilic Bacteria 253 7.6. Halophilic behavior of enzymes from the anaerobic halophilic Bacteria 264 7.7. Halophilic behavior of enzymes from the halophilic Eucarya 264 7.8. References 267 CHAPTER 8. ORGANIC COMPATIBLE SOLUTES 279 8.1. Organic osmotic solutes and their distribution 279 8.2. Compatible solutes in the domain Archaea 284 8.3. Compatible solutes in the domain Bacteria 286 8.4. Compatible solutes in the domain Eucarya 294 8.5. The mode of action of compatible solutes 297 8.6. References 299 CHAPTER 9. HALOPHILIC BACTERIOPHAGES AND HALOCINS 307 9.1. Bacteriophages of halophilic microorganisms 307 9.2. Halocins 316 9.3. References 319 CHAPTER 10. GENETICS AND GENOMICS OF HALOPHILIC ARCHAEA AND BACTERIA 323 10.1. Genetics of halophilic microorganisms - an historical survey 323 10.2. Genetics of halophilic Archaea 324 10.3. Genetics of halophilic Bacteria 343 10.4. References 348 CHAPTER 11. BIOTECHNOLOGICAL APPLICATIONS AND POTENTIALS OF 357 HALOPHILIC MICROORGANISMS 11.1. Introduction 357 11.2. Applications of halophlic Archaea 359 11.3. Applications of halophlic Bacteria 367 11.4. Applications of halophlic Eucarya 375 11.5. References 380 SECTION 3. HYPERSALINE ENVIRONMENTS AND THEIR BIOTA 391 INTRODUCTION 393 CHAPTER 12. GREAT SALT LAKE, UTAH 395 12.1. The lake and its setting 395 12.2. The microbial communities of the Great Salt Lake 400 12.3. Microbial isolates and their properties 407 12.4. Biogeochemical processes 409 12.5. References 415 x CHAPTER 13. THE DEAD SEA 419 13.1. The lake and its setting 419 13.2. Early studies on the biota of the Dead Sea 423 13.3. Dynamics of microbial blooms in the Dead Sea 424 13.4. Microbial isolates and their properties 431 13.5. Adaptations of the Dead Sea biota to the ionic composition of the lake 433 13.6. The nature of the species dominant in the archaeal blooms 434 13.7. Anaerobic processes in the Dead Sea sediments 434 13.8. Biology of the Dead Sea - expected future developments 435 13.9. References 436 CHAPTER 14. SOLAR SALTERNS 441 14.1. The saltern environment and its biota 441 14.2. Benthic microbial mats in the evaporation ponds 444 14.3. Microbial isolates and their properties 448 14.4. Approaches toward the identification of the dominant Archaea in saltern crystallizer ponds 451 14.5. Salinibacter and other halophilic Bacteria in saltern ponds 453 14.6. The red pigments in salten crystallizer ponds 454 14.7. Dynamics of archaeal and bacterial communities in saltern ponds 455 14.8. The importance of the saltern biota in the production of solar salt 459 14.9. References 462 CHAPTER 15. ALKALINE HYPERSALINE LAKES IN AFRICA AND ASIA 471 15.1. The Wadi Natrun lakes 472 15.2. Lake Magadi and other East-African soda lakes 478 15.3. Hypersaline soda lakes in Asia - chemical and biological characteristics 489 15.4. References 491 CHAPTER 16. MONO LAKE, CALIFORNIA, AND BIG SODA LAKE, NEVADA 495 16.1. Hypersaline lakes in the Great Basin of North America 495 16.2. Mono Lake, California 496 16.3. Big Soda Lake, Nevada 508 16.4. References 512 xi CHAPTER 17. MISCELLANEOUS HABITATS OF HALOPHILIC MICROORGANISMS – 517 FROM ANTARCTIC LAKES TO HYDROTHERMAL VENTS 17.1. Cold and hypersaline: Antarctic hypersaline lakes 517 17.2. Hot and hypersaline: Solar Lake (Sinai) and other warm brines 519 17.3. Seawater, deep sea brines and hydrothermal vents 525 17.4. Halophilic microorganisms in oil field brines 528 17.5. Halophiles in salt marshes, hypersaline lagoons and miscellaneous lakes 528 17.6. Hypersaline springs 531 17.7. Hypersaline soils 532 17.8. Wall paintings 532 17.9. Desert plants and animals 533 17.10. References 533 SECTION 4. EPILOGUE 541 CHAPTER 18. EPILOGUE:EVOLUTION OF HALOPHILES AND SURVIVAL 543 OF HALOPHILES ON EARTH AND IN SPACE 18.1. The evolutionary origin of halophiles 543 18.2. Long-term survival of halophiles in ancient salt crystals 545 18.3. Halophiles in space? 548 18.4. References 549 SECTION 5. SUPPLEMENT 553 METHODS FOR CULTIVATION AND HANDLING OF HALOPHILIC ARCHAEA AND 555 BACTERIA GLOSSARY OF LIMNOLOGICAL TERMS 559 ABOUT THE AUTHOR 561 ORGANISM INDEX 563 GEOGRAPHICAL INDEX 567 SUBJECT INDEX 571 FOREWORD "This water" he told me, "runs out to the eastern region, and flows into the Arabah; and when it comes into the sea, into the sea of foul waters [i.e., the Dead Sea], the water will become wholesome. Every living creature that swarms will be able to live wherever this stream goes; the fish will be very abundant once these waters have reached there. It will be wholesome, and everything will live wherever this stream goes. Fishermen shall stand beside it all the way from En-gedi to En-eglaim; it shall be a place for drying nets; and the fish will be of various kinds [and] most plentiful, like the fish of the Great Sea." Ezekiel’s prophecy (Ezekiel 47: 8-10) for revival and purification of the Dead Sea waters This new book on "Halophilic Microorganisms and their Environments" is the fifth volume in the COLE series (Cellular Origin and Life in Extreme Habitats (see: http://www.wkap.nl/prod/s/COLE).
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