ADAPTATION TO LIFE AT HIGH SALT 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
Printed on acid-free paper
All Rights Reserved © 2005 Springer No part of this work may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording or otherwise, without written permission from the Publisher, with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work.
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 saltern 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 salterns Carlos Pedrós-Alió 71
Isolation of viable haloarchaea from ancient salt deposits and application of fluorescent stains for in situ detection of halophiles 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
vii
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 halophile 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 halotolerance 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 Debaryomyces hansenii, a salt-loving yeast 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]
xi