ADAPTATION TO LIFE AT HIGH CONCENTRATIONS IN ARCHAEA, BACTERIA, AND EUKARYA Cellular Origin, Life in Extreme Habitats and Astrobiology

Volume 9

Series Editor: Joseph Seckbach The Hebrew University of Jerusalem, Israel Adaptation to Life at High Salt Concentrations in Archaea, Bacteria, and Eukarya

Edited by Nina Gunde-Cimerman Biotechnical Faculty, Department of Biology, University of Ljubljana, Slovenia Aharon Oren The Institute of Life Sciences and the Moshe Minerva Center for Marine Biogeochemistry, The Hebrew University of Jerusalem, Israel and Ana Plemenitaš Institute of Biochemistry, University of Ljubljana, Slovenia A C.I.P. Catalogue record for this book is available from the Library of Congress.

ISBN-10 1-4020-3632-9 (HB) ISBN-10 1-4020-3633-7 (e-book) ISBN-13 978-1-4020-3632-3 (HB) ISBN-13 978-1-4020-3633-0 (e-book)

Published by Springer, P.O. Box 17, 3300 AA Dordrecht, The Netherlands. www.springeronline.com

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Printed in the Netherlands. TABLE OF CONTENTS

Foreword Joseph Seckbach xi

Introduction Nina Gunde-Cimerman, Aharon Oren and Ana Plemenitaš 1

Section I. The environments and their diversity 7

Microbial diversity of Great Salt Lake Bonnie K. Baxter, Carol D. Litchfield, Kevin Sowers, Jack D. Griffith, Priya Arora DasSarma and Shiladitya DasSarma 9

Microbial communities in the Dead Sea – past, present and future Aharon Oren, Ittai Gavrieli, Jonah Gavrieli, Marco Kohen, Joseph Lati and Mordehay Aharoni 27

Microscopic examination of microbial communities along a salinity gradient in evaporation ponds: a ‘halophilic safari’ Aharon Oren 41

The microbial diversity of a solar saltern on San Francisco Bay Carol D. Litchfield, Masoumeh Sikaroodi and Patrick M. Gillivet 59

Diversity of microbial communities: the case of solar Carlos Pedrós-Alió 71

Isolation of viable haloarchaea from ancient salt deposits and application of fluorescent stains for in situ detection of in hypersaline environmental samples and model fluid inclusions Stefan Leuko, Andrea Legat, Sergiu Fendrihan, Heidi Wieland, Christian Radax, Claudia Gruber, Marion Pfaffenhuemer, Gerhard Weidler and Helga Stan-Lotter 91 vi

Hydrocarbon degradation under hypersaline conditions. Some facts, some experiments and many open questions Heiko Patzelt 105

The relevance of halophiles and other extremophiles to Martian and extraterrestrial environments Joseph Seckbach 123

Halophiles: a terrestrial analog for life in brines on Mars – Halophiles on Mars Rocco L. Mancinelli 137

Section II. Archaea 149

Comparative genomic survey of information transfer systems in two diverse extremely halophilic Archaea, Halobacterium sp. strain NRC-1 and Haloarcula marismortui Brian R. Berquist, Jeetendra Soneja and Shiladitya DasSarma 151

Walsby’s square archaeon; it’s hip to be square but even more hip to be culturable Henk Bolhuis 185

Gene regulation and the initiation of translation in halophilic Archaea Felicitas Pfeifer, Peter Zimmermann, Sandra Scheuch and Simone Sartorius-Neef 201

Protein translation, targeting and translocation in Haloferax volcanii Jerry Eichler, Gabriela Ring, Vered Irihimovitch, Tovit Lichi, Irit Tozik and Zvia Konrad 217

Enzymes of halophilic Archaea. Recent findings on ureases and nucleoside diphosphate kinases Toru Mizuki, Ron Usami, Masayuki Kamo, Masaru Tanokura and Masahiro Kamekura 227

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Osmoadaptation in methanogenic Archaea: recent insights from a genomic perspective Katharina Pflüger, Heidi Wieland and Volker Müller 239

Section III. Bacteria 253

Salinibacter ruber: genomics and biogeography Josefa Antón, Arantxa Peña, Maria Valens, Fernando Santos, Frank-Oliver Glöckner, Margarete Bauer, Joaquín Dopazo, Javier Herrero, Ramon Rosselló-Mora and Rudolf Amann 255

What we can deduce about metabolism in the moderate Chromohalobacter salexigens from its genomic sequence Laszlo N. Csonka, Kathleen O’Connor, Frank Larimer, Paul Richardson, Alla Lapidus, Adam D. Ewing, Bradley W. Goodner and Aharon Oren 267

K+ transport and its role for osmoregulation in a halophilic member of the Bacteria domain: characterization of the K+ uptake systems from Halomonas elongata Hans-Jörg Kunte 287

The chloride regulon of Halobacillus halophilus: a novel regulatory network for salt perception and signal transduction in bacteria Volker Müller and Stephan H. Saum 301

Biosynthesis of the compatible solute mannosylglycerate from hyperthermophiles to mesophiles. Genes, enzymes and evolutionary perspectives Milton S. da Costa and Nuno Empadinhas 311

Genes and enzymes of ectoine biosynthesis in the haloalkaliphilic obligate methanotroph “Methylomicrobium alcaliphilum 20Z” Alexander S. Reshetnikov, Valentina N. Khmelenina, Ildar I. Mustakhimov, Yana V. Ryzhmanova and Yuri A. Trotsenko 327 viii

Halophilic Archaea and Bacteria as a source of extracellular hydrolytic enzymes Antonio Ventosa, Cristina Sánchez-Porro, Sara Martín and Encarnación Mellado 337

Biopolyester production: halophilic microorganisms as an attractive source Jorge Quillaguamán, Bo Mattiasson and Rajni Hatti-Kaul 355

Section IV. Fungi 369

Relation of to human pathogenicity in the fungal tree of life: an overview of ecology and evolution under stress G. Sybren de Hoog, Polona Zalar, Bert Gerrits van den Ende and Nina Gunde-Cimerman 371

Halotolerant and halophilic fungi from coastal environments in the Arctics Nina Gunde-Cimerman, Lorena Butinar, Silva Sonjak, Martina Turk, Viktor Uršiþ, Polona Zalar and Ana Plemenitaš 397

Halotolerant and halophilic fungi and their extrolite production Jens C. Frisvad 425

Introducing hansenii, a salt-loving José Ramos 441

Cellular responses in the halophilic black yeast Hortaea werneckii to high environmental salinity Ana Plemenitaš and Nina Gunde-Cimerman 453

Halotolerance and lichen symbioses Martin Grube and Juliane Blaha 471

Section V. Algae 489

A century of Dunaliella research: 1905-2005 Aharon Oren 491 ix

Molecular determinants of protein halotolerance: structural and functional studies of the extremely salt tolerant carbonic anhydrases from Dunaliella salina Lakshmane Premkumar, Michal Volkovitsky, Irena Gokhman, Joel L. Sussman and Ada Zamir 503

Section VI. Protozoa 517

Heterotrophic protozoa from hypersaline environments Gwen Hauer and Andrew Rogerson 519

Heterotrophic flagellates in hypersaline waters Byung C. Cho 541

Section VII. Viruses 551

Haloviruses and their hosts Mike L. Dyall-Smith, David G. Burns, Helen M. Camakaris, Peter H. Janssen, Brendan E. Russ and Kate Porter 553

Subject Index 565

Organism Index 569

Author Index 575

FOREWORD

Salt is an essential requirement of life. Already from ancient times (e.g., see the books of the Bible) its importance in human life has been known. For example, salt symbolizes destruction (as in Sodom and Gomorra), but on the other hand it has been an ingredient of every sacrifice during the Holy Temple periods. Microbial life in concentrated salt solutions has fascinated scientists since its discovery. Recently there have been several international meetings and books devoted entirely to halophiles. This book includes the proceedings of the “Halophiles 2004” conference held in Ljubljana, Slovenia, in September 2004 (www.uni- lj.si/~bfbhaloph/index.html). This meeting was attended by 120 participants from 25 countries. The editors have selected presentations given at the meeting for this volume, and have also invited a number of contributions from experts who had not been present in Ljubljana. This book complements “Halophilic Microorganisms”, edited by A. Ventosa and published by Springer-Verlag (2004), “Halophilic Microorganism and their Environments” by A. Oren (2002), published by Kluwer Academic Publishers as volume 5 of “Cellular Origins, Life in Extreme Habitats and Astrobiology” (COLE), and “Microbiology and Biogeochemistry of Hypersaline Environments” edited by A. Oren, and published by CRC Press, Boca Raton (1999). Salt-loving (halophilic) microorganisms grow in salt solutions above seawater salinity (~3.5% salt) up to saturation ranges (i.e., around 35% salt). High concentrations of salt occur in natural environments (e.g., in the Dead Sea and the Great Salt Lake, Utah) and in man-made hypersaline environments such as solar salterns. The research of halophiles covers all three domains of life, i.e., Archaea, Bacteria, and Eukarya. This multi-author review has been edited by Professors Nina Gunde-Cimerman, Aharon Oren and Ana Plemenitaš. It is volume 9 of the COLE book series [“Cellular Origins, Life in Extreme Habitats and Astrobiology”, edited by J. Seckbach, now published by Springer] (www.springeronline.com). It covers most recent research on halophiles in chapters contributed by experts in this field. I wish to thank the editors for suggesting the publication of this volume in the framework of the COLE series and for editing all the chapters of this book.

January 2005

Joseph Seckbach Chief Editor of the COLE book series The Hebrew University of Jerusalem

E-mail: [email protected]

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