Seckbach_FM.qxd 17/8/07 1:04 PM Page i ALGAE AND CYANOBACTERIA IN EXTREME ENVIRONMENTS Seckbach_FM.qxd 17/8/07 1:04 PM Page ii Cellular Origin, Life in Extreme Habitats and Astrobiology Volume 11 Series Editor: Joseph Seckbach The Hebrew University of Jerusalem,Israel The titles published in this series are listed at the end of this volume. Seckbach_FM.qxd 17/8/07 1:04 PM Page iii Algae and Cyanobacteria in Extreme Environments Edited by J. Seckbach The Hebrew University of Jerusalem, Israel Seckbach_FM.qxd 17/8/07 1:04 PM Page iv A C.I.P.Catalogue record for this book is available from the Library of Congress. ISBN 978-1-4020-6111-0 (HB) ISBN 978-1-4020-6112-7 (e-book) Published by Springer, P.O.Box 17,3300 AA Dordrecht,The Netherlands. www.springer.com LEGENDSFORTHECOVERPICTURE An arrangement of 44 diatoms surrounded by images of cyanobacteria and chlorophyte algae. The diatoms include species from the genera Actinoptychus, Amphitetras, Aulacodiscus, Caloneis, Cocconeis, Cymatopleura, Cymbella, Didymosphenia, Diploneis, Gyrosigma, Hemiaulus, Mastogloia, Melosira, Navicula, Neidium, Paralia, Pleurosigma, Rhabdonema, Stauroneis, Stictodiscus, Surirella, Synedra, Tetracyclus, Triceratium, and Trinacria. The algae bordering the diatoms include (from top left corner): the desmid Staurastrum artiscon,the cyanobacterium Anabaena,the desmid Micrasterias hardyii,the coiled filaments of Spirogyra,the tapered cork screw-like filaments of the cyanobacterium Spirulina, and the coiled filaments of Zygnema. Border algae images are contributed by Dr. Gordon W. Beakes, Newcastle University, UK. The diatom arrangement and pho- tomicrograph, and the composite image of all algae, are by Dr. Stephen S. Nagy (MD), Montana Diatoms,USA. Printed on acid-free paper All Rights Reserved © 2007 Springer No part ofthis 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 mate- rial supplied specifically for the purpose of being entered and executed on a computer system,for exclusive use by the purchaser of the work. Seckbach_FM.qxd 17/8/07 1:04 PM Page v TABLE OF CONTENTS1 Foreword/Richard W.Castenholz. . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix Preface/Joseph Seckbach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xv Introduction to the Algal World/Meltem Conk Dalay . . . . . . . . . . . . . xix Acknowledgements/Joseph Seckbach. . . . . . . . . . . . . . . . . . . . . . . . . . xxiii List of Authors and their Addresses . . . . . . . . . . . . . . . . . . . . . . . . . . xxv PART 1: GENERAL INTRODUCTION Oxygenic Photosynthetic Microorganisms in Extreme Environments: Possibilities and Limitations [Seckbach,J.and Oren,A.] . . . . . . . 5 PART 2: PHOTOTROPHS AT HIGH AND LOW LIGHT Effects of Ultraviolet Radiation on Cyanobacteria and Their Protective Mechanisms [Pattanaik,B.etal.]. . . . . . . . . 31 The Hidden Life of Algae Underground [Reisser,W.] . . . . . . . . . . . . . 49 Meromictic Lakes as Habitats for Protists:Life in the Chemocline and Below? [Klaveness,D.and Løvhøiden,F.] . . . . . . . . . . . . . . . . 61 Marine Phototrophs in the Twilight Zone [Stambler,N.and Dubinsky,Z.]. . . . . . . . . . . . . . . . . . . . . . . . . . . 81 PART 3: PHOTOTROPHS IN THE MARINE ENVIRONMENT Biology of the Chlorophyll D-Containing Cyanobacterium Acaryochloris marina[Kühl,M.etal.]. . . . . . . . . . . . . . . . . . . . . . 103 Phylogenetics,Molecular Biology and Ecological Impacts of a Group of Highly Unusual Protists: The Dinoflagellates [Murray,S.]. . . . . . . . . . . . . . . . . . . . . . . . . . 127 1The editor thanks Professors Aharon Oren and Richard Castenholz for their suggestions in the above division of the chapters into sections. v Seckbach_FM.qxd 17/8/07 8:19 PM Page vi vi TABLE OF CONTENTS Diatoms:Living in a Constructal Environment [Sterrenburg,F.A.S.etal.]. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143 The Margin of the Sea:Survival at the Top of the Tides [Garbary,D.J.]. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 175 Seaweeds on the Abrasion Platforms of the Intertidal Zone of Eastern Mediterranean Shores [Einav,R.and Israel,A.]. . . . . . 195 Status of Mangrove Ecosystem:Exploring the Potential Role of Cyanobacteria in Restoration and Afforestation [Sundararaman,M.etal.] . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 211 Intertidal Sandy Beaches as a Habitat Where Plastid Acquisition Processes are Ongoing [Okamoto,N.and Inouye,I.]. . . . . . . . . . . 227 Hydrochemical Key to the Genesis of Calcareous Nonlaminated and Laminated Cyanobacterial Microbialites [Kempe,S.and Kazmierczak,J.] . . . . . . . . . . . . . . . 241 Soil and Freshwater Micro-Algae as a Food Source for Invertebrates in Extreme Environments [Lukeˇsová,A.and Frouz,J.] . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 267 PART 4: PHOTOTROPHS IN COLD ENVIRONMENTS Cold Tolerance in Cyanobacteria and Life in the Cryosphere [Vincent,W.F.]. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 289 Cyanobacteria in Antarctic Lake Environments: A Mini-Review [Singh,S.M.and Elster,J.]. . . . . . . . . . . . . . . . . . 305 Green Cryosestic Algae [Komárek,J.and Nedbalová,L.]. . . . . . . . . . . 323 Psychrophilic Diatoms:Mechanisms for Survival in Freeze–Thaw Cycles [Mock,T.and Junge,K.] . . . . . . . . . . . . . 345 Algae at Extreme Low Temperatures:The Cryobank [Benson,E.E.etal.]. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 367 PART 5: PHOTOTROPHS IN HOT ALKALINE AND ACIDIC ENVIRONMENTS AND NON-THERMAL ACIDIC HABITATS Cyanidiophyceae:Looking Back–Looking Forward [Pinto,G.]. . . . . . 389 Diversity of the Cosmopolitan Thermophile Mastigocladus laminosusat Global,Regional and Local Scales [Miller,S.R.] . . . 401 The Thermophilic Cyanobacteria of the Zerka Ma’in Thermal Springs in Jordan [Ionescu,D.etal.]. . . . . . . . . . . . . . . . . . . . . . . 413 Iron-Tolerant Cyanobacteria:Implications for Astrobiology [Brown,I.etal.]. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427 Extreme Acidophiles:Freshwater Algae Associated with Acid Mine Drainage [Novis,P.M.and Harding,J.S.] . . . . . . 445 Seckbach_FM.qxd 17/8/07 8:19 PM Page vii TABLE OF CONTENTS vii Eukaryotic Community Structure from Río Tinto (Sw,Spain), a Highly Acidic River [Aguilera,A.etal.]. . . . . . . . . . . . . . . . . . . 467 Species Composition of Cyanidiales Assemblages in Pisciarelli (Campi Flegrei,Italy) and Description of Galdieria phlegreasp.nov.[Pinto,G.etal.]. . . . . . . . . . . . . . . . . . 489 A Genomics Approach to Understanding the Biology of Thermo-Acidophilic Red Algae [Weber,A.P.M.etal.]. . . . . . . 505 Enigmatic Archaeal and Eukaryotic Life at Hydrothermal Vents and in Marine Subsurface Sediments [Teske,A.]. . . . . . . . . 521 PART 6: PHOTOTROPHS UNDER WATER STRESS: DRY AND HYPERSALINE ENVIRONMENTS North American Desert Microbiotic Soil Crust Communities: Diversity Despite Challenge [Flechtner,V.R.] . . . . . . . . . . . . . . . . 539 Chroococcidiopsisfrom Desert to Mars [Grilli Caiola,M.and Billi,D.] 555 Chlorophyta on Land:Independent Lineages of Green Eukaryotes from Arid Lands [Lewis,L.A.] . . . . . . . . . . . . . . . . . . . . . . . . . . . 571 Aeroterrestrial Algae Growing on Man-Made Surfaces: What are the Secrets of their Ecological Success? [Karsten,U.etal.]. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 585 The Systematics of Subaerial Algae [Lopez-Bautista,J.M.etal.]. . . . . 601 Diversity,Distribution and Ecology of Green Algae and Cyanobacteria in Urban Habitats[Rindi,F.] . . . . . . . . . . . . . 621 Diversity of Organic Osmotic Compounds and Osmotic Adaptation in Cyanobacteria and Algae [Oren,A.] . . . . . . . . . . . 641 PART 7: ADAPTATION OF ALGAE TO CHANGING ENVIRONMENTS Cyanobacteria:Diversity and Versatility,Clues to Life in Extreme Environments [Stal,L.J.] . . . . . . . . . . . . . . . . . . . . . . 661 Life in a Hypervariable Environment:Algae of the Great Salt Plains of Oklahoma,USA [Henley,W.J.etal.] . . . . . . . . . . . 683 PART 8: OTHER MICROORGANISMS AND EXTREME HABITATS The Fate of Biological Materials in Acidic Environments of the Río Tinto,Southwestern Spain [Fernández-Remolar,D.C.etal.]. . 699 Seckbach_FM.qxd 17/8/07 8:19 PM Page viii viii TABLE OF CONTENTS Deep-Sea Microbial Eukaryotes in Anoxic,Microoxic, and Sulfidic Environments [Edgcomb,V.P.etal.] . . . . . . . . . . . . . 713 Fungal Associations at the Cold Edge of Life [Onofri,S.etal.] . . . . . 739 The Early Earth’s Record of Supposed Extremophilic Bacteria and Cyanobacteria,at 3.8 to 2.5 Ga [Altermann,W.] . . . 761 PART 9: OUTLOOK-SUMMARY Algae and Cyanobacteria Under Environmental Extremes: Final Comments [Seckbach,J.etal.] . . . . . . . . . . . . . . . . . . . . . . 783 Organism Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 787 Subject Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 799 Author Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 809 Seckbach_FM.qxd 17/8/07 1:04 PM Page ix FOREWORD This volume encompasses a great diversity of subjects as well as authors,most of whom are well recognized and established in their fields and others who are younger,upcoming scientists of whom we will hear more in the future.The subject is extremophiles,and is almost entirely focused on photosynthetic microbes.It is a complementary and updated version of a volume of similar subject matter published in 2001 (Algae and Extreme Environments:Ecology and Physiology,eds. J.Elster,J.Seckbach,W.F.Vincent and O.Lhotsky,Nova Hedwigia,Beiheft 123: 1–602. Schweizerbart’sche Verlagsbuchhandlung, D-70176 Stuttgart. http://www. schweizerbart.de/pubs/books/bo/novahedwig-051012300-desc.ht,Berlin/Stuttgart, 602 pp.). Few of the authors of the present volume were involved in the earlier publication,and many of the subjects are quite different. The studies of extremophiles have increased almost exponentially in the last several years,mainly because of the interest in early life on this planet and possi- ble life (past or present) on others.This has necessitated the creation of a new and well-received journal,Extremophiles(Volume 1,1997 to present).Unfortunately, few of the papers published in this journal to date have focused on phototrophs. Papers on tolerance to environmental extremes by phototrophic microorganisms are also frequently found in a number of journals,including Journal ofPhycology, Applied and Environmental Microbiology,Environmental Microbiology,Microbial Ecology,Archives ofMicrobiology,and several others,and,of course,in the series of volumes entitled “Cellular Origin,Life in Extreme Habitats and Astrobiology” (www.springer.com/series/5775) edited by Joseph Seckbach. The current volume is divided into nine subject areas in addition to an open- ing section: General introductory chapter (1), (2) Phototrophs at high and low light, (3) Phototrophs in the marine environment, (4) Phototrophs in cold envi- ronments, (5) Phototrophs in hot alkaline and acidic environments and non-thermal acidic habitats, (6) Phototrophs under water stress: dry and hyper- saline environments, (7) Adaptability to changing environments, (8) Other microorganisms and extreme habitats,and (9) Outlook. We need to remember that phototrophs, except for a few, do not generally extend as far into some extreme environments as do the non-photosynthetic Bacteria and Archaea. With respect to upper temperature limits, a few Cyanobacteria and Chloroflexi extend to the lower 70°Cs which demarks the upper boundary for a few unique organisms of each of these phyla, and conse- quently the upper temperature limit for chlorophyll- or bacteriochlorophyll-based photosynthesis (a limit known and not disputed for many decades).With respect to upper salinity limits, there too the non-photosynthetic Bacteria and Archaea dominate the picture, but there are exceptions. Some phototrophic purple ix