Table Of ContentANOXIA
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
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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 O depletion or to an extreme form of “low oxygen.” Both terms
2
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 O . Microorganisms that
2
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
temperature or concentration stratifi cation, such as in denser hypersaline waters.
Anoxic conditions will occur if the rate of oxidation of organic matter is greater
than the supply of dissolved oxygen. Anoxic waters are a natural phenomenon,
and have occurred throughout the geological history. At present, for example,
anoxic basins exist in the Baltic and Mediterranean Seas and elsewhere.
Eutrophication of freshwater lakes and marine environments often causes
increase in the extent of the anoxic areas. Decay of phytoplankton blooms also
intensifi es the anoxic conditions in a water body. Although algae produce oxygen in
the daytime via photosynthesis, during the night hours they continue to undergo
cellular respiration and can therefore deplete available oxygen. In addition, when
algal blooms die off, oxygen is further used during bacterial decomposition of the
dead algal cells. Both of these processes can result in a signifi cant depletion of
dissolved oxygen in the water, creating hypoxic conditions or a dead zone
(low-oxygen areas).
Among the eukaryotic anaerobes one could fi nd protists that live in hypersaline
environments (up to 365 g/l NaCl), for example, the groups of ciliates, dinofl agellates,
choanofl agellates, and other marine protozoa. We are aware of some eukaryotes
that act in anaerobic conditions such as the yeast that ferments sugars to ethanol
and CO , wine fermentation, and in the baking process. Second, the protozoa
2
(e.g., ciliates) in the rumen of cows and other ruminant animals act in anaerobic
ix
x INTRODUCTION TO ANOXIA
conditions. In some anoxic single eukaryotic cells, the mitochondria are replaced
by hydrogenosomes, or the mitochondrion is adapted as an unusual organelle
structure for the anaerobic metabolism.
Lately a group of metazoa was detected living in a permanently anoxic
environment in the sediments of the deep hypersaline basin 3.5 km below the
surface of the Mediterranean Sea. Others have detected eukaryotes in anoxic
areas of the Black Sea and near Costa Rica. Some Foraminifera are found living
in oxygen-free zones, such as in Swedish Fjords, in the Cariaco and Santa Barbara
Basin, the Black Sea, or off Namibia.
In the severely cold winters of the Northern Arctic zones, there are plants
that can survive under a covering of ice which completely prevents access to
oxygen. Any remaining oxygen in the soil atmosphere is consumed by microbial
activity. There is therefore a total cessation of aerobic metabolism for several
months in the overwintering organs, such as tubers and underground stems. The
ability of these perennial organs to maintain viable buds throughout an anoxic
winter enables the plants to grow new roots and shoots when aerobic metabolism
is resumed on thawing in spring (see Crawford in this volume). We know also that
in certain species seed germination can take place in anaerobic conditions.
Similarly, the tolerance of insects to anoxia has also been recorded in this volume
(Hoback, in this volume).
Tardigrades (segmented polyextremophilic eukaryotic animals, less than
1 mm in length) can survive and exhibit extraordinary tolerance to several extreme
environments. The results with anhydrobiotic tardigrades strongly suggest that
these invertebrate animals can survive even in anoxic environments in outer space.
It seems that oxygen supply to the tardigrades causes critical damage to these
anhydrobiotic animals under such conditions (Horikawa in this volume).
The present topic of A NOXIA: Evidence for Eukaryote Survival and
Paleontological Strategies is timely and exciting and we now present it in this
volume, which is aimed at biological researchers of ecology and biodiversity, to
astrobiologists, to readers interested in extreme environments, and also paleoe-
cologists and paleontologists (and some sedimentologists). This volume is
number 21 of the C ellular Origin, Life in Extreme Habitats and Astrobiology
[COLE] series, [www.springer.com/series/5775]. It contains 32 chapters contri-
buted by 71 authors from 13 countries (given here in alphabetical order):
Austria, Canada, Denmark, France, Germany, Israel, Italy, Japan, Peru, the
Netherlands, Ukraine, the United Kingdom, and the USA. We availed ourselves
of 25 external referees in addition to our peer reviewers to evaluate the chapters.
It is our hope that our readers will enjoy this book in which we invested so much
enthusiasm and effort.
The author thanks Professors Aharon Oren and David Chapman for their
constructive suggestions to improve this Introduction.
Joseph Seckbach The Hebrew University of Jerusalem
Jerusalem, Israel
