ANOXIA Cellular Origin, Life in Extreme Habitats and Astrobiology Volume 21 Series Editor: Joseph Seckbach The Hebrew University of Jerusalem, Israel For further volumes: http://www.springer.com/series/5775 Anoxia Evidence for Eukaryote Survival and Paleontological Strategies Edited by Alexander V. Altenbach Ludwig-Maximilians-University, Munich, Germany Joan M. Bernhard Wood Hole Oceanographic Institution, MA, USA and Joseph Seckbach The Hebrew University of Jerusalem, Israel Editors Alexander V. Altenbach Joan M. Bernhard Department for Earth and Environmental Geology and Geophysics Department Science, and GeoBio-Center Wood Hole Oceanographic Institution Ludwig-Maximilians-University MS52, Woods Hole, MA 02543 Richard-Wagner-Str. 10 USA 80333 Munich [email protected] Germany [email protected] Joseph Seckbach P.O. Box 1132 90435 Efrat Israel [email protected] ISSN 1566-0400 ISBN 978-94-007-1895-1 e-ISBN 978-94-007-1896-8 DOI 10.1007/978-94-007-1896-8 Springer Dordrecht Heidelberg London New York Library of Congress Control Number: 2011935457 © Springer Science+Business Media B.V. 2012 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, microfi lming, recording or otherwise, without written permission from the Publisher, with the exception of any material supplied specifi cally for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com) TABLE OF CONTENTS Introduction/Joseph Seckbach ............................................................. ix Stepping into the Book of Anoxia and Eukaryotes/The Editors ....... xi List of Authors and their Addresses ................................................... xxi List of External Reviewers and Referees ............................................ xxix Acknowledgment to Authors, Reviewers, and any Special People Who Assisted ................................................................................. xxxiii PART 1: GENERAL INTRODUCTION Anaerobic Eukaryotes [Fenchel, T.] ..................................................... 3 Biogeochemical Reactions in Marine Sediments Underlying Anoxic Water Bodies [Treude, T.] ................................................. 17 Diversity of Anaerobic Prokaryotes and Eukaryotes: Breaking Long-Established Dogmas [Oren, A.] .......................... 39 PART 2: FUNCTIONAL BIOCHEMISTRY The Biochemical Adaptations of Mitochondrion-Related Organelles of Parasitic and Free-Living Microbial Eukaryotes to Low Oxygen Environments [Tsaousis, A.D. et al.] ..................................................................... 51 Hydrogenosomes and Mitosomes: Mitochondrial Adaptations to Life in Anaerobic Environments [de Graaf, R.M. and Hackstein, J.H.P.] ................................................................... 83 Adapting to Hypoxia: Lessons from Vascular Endothelial Growth Factor [Levy, N.S. and Levy, A.P.] .................................. 113 v vi TABLE OF CONTENTS PART 3: MANAGING ANOXIA Magnetotactic Protists at the Oxic–Anoxic Transition Zones of Coastal Aquatic Environments [Bazylinski, D.A. et al.] .................................................................. 131 A Novel Ciliate (Ciliophora: Hypotrichida) Isolated from Bathyal Anoxic Sediments [Beaudoin, D.J. et al.] ...................................... 145 The Wood-Eating Termite Hindgut: Diverse Cellular Symbioses in a Microoxic to Anoxic Environment [Dolan, M.F.] ................................................................................. 155 Ecological and Experimental Exposure of Insects to Anoxia Reveals Surprising Tolerance [Hoback, W.W.] ............................. 167 The Unusual Response of Encysted Embryos of the Animal Extremophile, Artemia franciscana, to Prolonged Anoxia [Clegg, J.S.] .................................................................................... 189 Survival of Tardigrades in Extreme Environments: A Model Animal for Astrobiology [Horikawa, D.D.].................................. 205 Long-Term Anoxia Tolerance in Flowering Plants [Crawford, R.M.M.] ........................................................... 219 PART 4: FORAMINIFERA Benthic Foraminifera: Inhabitants of Low-Oxygen Environments [Koho, K.A. and Piña-Ochoa, E.] .................................................. 249 Ecological and Biological Response of Benthic Foraminifera Under Oxygen-Depleted Conditions: Evidence from Laboratory Approaches [Heinz, P. and Geslin, E.] ...................... 287 The Response of Benthic Foraminifera to Low-Oxygen Conditions of the Peruvian Oxygen Minimum Zone [Mallon, J. et al.] ............................................................................ 305 Benthic Foraminiferal Communities and Microhabitat Selection on the Continental Shelf Off Central Peru [Cardich, J. et al.] ........................................................................... 323 PART 5: ZONES AND REGIONS Living Assemblages from the “Dead Zone” and Naturally Occurring Hypoxic Zones [Buck, K.R. et al.] .............................. 343 TABLE OF CONTENTS vii The Return of Shallow Shelf Seas as Extreme Environments: Anoxia and Macrofauna Reactions in the Northern Adriatic Sea [Stachowitsch, M. et al.] ........................................... 353 Meiobenthos of the Oxic/Anoxic Interface in the Southwestern Region of the Black Sea: Abundance and Taxonomic Composition [Sergeeva, N.G. et al.] ............................................. 369 The Role of Eukaryotes in the Anaerobic Food Web of Stratifi ed Lakes [Saccà, A.] ...................................................... 403 The Anoxic Framvaren Fjord as a Model System to Study Protistan Diversity and Evolution [Stoeck, T. and Behnke, A.] ........................................................... 421 Characterizing an Anoxic Habitat: Sulfur Bacteria in a Meromictic Alpine Lake [Fritz, G.B. et al.]...................................................... 449 Ophel, the Newly Discovered Hypoxic Chemolithotrophic Groundwater Biome: A Window to Ancient Animal Life [Por, F.D.] ....................................................................................... 463 Microbial Eukaryotes in the Marine Subsurface? [Edgcomb, V.P. and Biddle, J.F.] .................................................... 479 PART 6: MODERN ANALOGS AND TEMPLATES FOR EARTH HISTORY On The Use of Stable Nitrogen Isotopes in Present and Past Anoxic Environments [Struck, U.]................................................ 497 Carbon and Nitrogen Isotopic Fractionation in Foraminifera: Possible Signatures from Anoxia [Altenbach, A.V. et al.] ................................................................... 515 The Functionality of Pores in Benthic Foraminifera in View of Bottom Water Oxygenation: A Review [Glock, N. et al.] .............................................................................. 537 Anoxia-Dysoxia at the Sediment-Water Interface of the Southern Tethys in the Late Cretaceous: Mishash Formation, Southern Israel [Almogi-Labin, A. et al.] ..................................... 553 Styles of Agglutination in Benthic Foraminifera from Modern Santa Barbara Basin Sediments and the Implications of Finding Fossil Analogs in Devonian and Mississippian Black Shales [Schieber, J.] ............................................................. 573 Did Redox Conditions Trigger Test Templates in Proterozoic Foraminifera? [Altenbach, A.V. and Gaulke, M.] ......................... 591 The Relevance of Anoxic and Agglutinated Benthic Foraminifera to the Possible Archean Evolution of Eukaryotes [Altermann, W. et al.] ..................................................................... 615 viii TABLE OF CONTENTS Organism Index ........................................................................................... 631 Subject Index .............................................................................................. 639 Author Index .............................................................................................. 647 INTRODUCTION TO ANOXIA: EVIDENCE FOR EUKARYOTE SURVIVAL AND PALEONTOLOGICAL STRATEGIES Research in anoxic environments is a relatively new and rapidly growing branch of science that is of general interest to many students of diverse microbial com- munities. The term anoxia means absence of atmospheric oxygen, while the term hypoxia refers to O2 depletion or to an extreme form of “low oxygen.” Both terms anoxia and hypoxia are used in various contexts. It is accepted that the initial microorganisms evolved anaerobically and thrived in an atmosphere without oxygen. The rise of atmospheric oxygen occurred ~2.3 bya through the photosynthesis process of cyanobacteria which “poisoned” the environment by the release of toxic O2 . Microorganisms that could adapt to the oxygenated environment survived and some of them evolved further to the eukaryotic kingdom in an aerobic atmosphere, while others vanished or escaped to specifi c anaerobic niches where they were protected. Most of the anaerobes are prokaryotes, while some are also within the Eukaryan kingdom. Those latter organisms are the focus of this new volume. Anaerobic areas of marine or fresh water that are depleted of dissolved oxygen have restricted water exchange. In most cases, oxygen is prevented from reaching the deeper levels by a physical barrier (e.g., silt or mud) as well as by