Anoxia Evidence for Eukaryote Survival and Paleontological Strategies pdf

ANOXIA
Cellular Origin, Life in Extreme Habitats and Astrobiology
Volume 21
Series Editor:
Joseph Seckbach
The Hebrew University of Jerusalem, Israel
For further volumes:
/>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
Department for Earth and Environmental
Science, and GeoBio-Center
Ludwig-Maximilians-University
Richard-Wagner-Str. 10
80333 Munich
Germany

Joseph Seckbach
P.O. Box 1132
90435 Efrat

Israel

Joan M. Bernhard
Geology and Geophysics Department
Wood Hole Oceanographic Institution
MS52, Woods Hole, MA 02543
USA

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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v
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
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.] 13 1
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.] 16 7

The Unusual Response of Encysted Embryos of the Animal
Extremophile, Artemia franciscana, to Prolonged Anoxia
[Clegg, J.S.] 1 89
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.] 3 2 3
PART 5:
ZONES AND REGIONS
Living Assemblages from the “Dead Zone” and Naturally
Occurring Hypoxic Zones [Buck, K.R. et al.] 343
vii
TABLE OF CONTENTS
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.] 51 5
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.] 5 73
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.] 6 1 5
viii
TABLE OF CONTENTS
Organism Index 631
Subject Index 639
Author Index 647
ix
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
2
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 O
2
. 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
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
2
, wine fermentation, and in the baking process. Second, the protozoa
(e.g., ciliates) in the rumen of cows and other ruminant animals act in anaerobic
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 ANOXIA: 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 Cellular 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
xi
STEPPING INTO THE BOOK OF ANOXIA AND EUKARYOTES
With this book, the editors, authors, and reviewers cooperated in promoting the
debate on the persistence of eukaryotes in anoxic environments and newly disco-
vered adaptations of eukaryotes in oxygen-depleted habitats. Also with this book,
we wish to attract scientists and students from all types of science to conduct
research in low-level oxygen to truly anoxic environments. We not only seek to
provide overviews and basics that lead to a better understanding, but also want to
communicate the endeavor and fascination involved in this research. The six parts
of the book span a broad range from molecular biology to fi eld research, from
environmental monitoring to paleoecology. Hopefully, this may also enhance
interest and cooperation on interdisciplinary grounds. Most of the questions
raised are under discussion at present, a positive sign for frontier research where
rapid developments transpire.
Thriving eukaryotes and anoxic environments were considered quite incom-
patible for a long time. In Part I, basics on eukaryotes recovered from anoxic
environments are summarized (Fenchel), and principles of biogeochemical activities

near the redoxcline are outlined (Treude). The comparison of common former
considerations about anoxic life and our present knowledge offers insight into the
possible revision of some dogmatic views (Oren).
Part II exemplifi es the biochemical pathways required for eukaryotes under
oxygen stress or absence of molecular oxygen. This section covers the biochemical
adaptation to low-oxygen environments (Tsaousis), and an overview on the
specifi c function of hydrogenosomes and mitosomes in anaerobes (De Graaf and
Hackstein). The present debate about eukaryotic cell evolution is ultimately
linked to the issue of how mitochondria originated and evolved. In the context of
a classical view, the Archaea and the Eukarya have a common ancestor.
Alternative views propose that the Eukarya evolved directly from the archaeal
lineage. The defi nition of modern anaerobic eukaryotes as remnants of the one
or other lineage is an as-yet-unresolved question. One possible implication in this
context is of utmost importance for evolutionary biology: anaerobiosis in extant
eukaryotes would be either a late adaptation developed by obligate aerobic
eukaryotes, or an omnipresent ability since the most ancestral lineage. A compre-
hensive overview of pathways for the adaptation to anoxic conditions are explained
and discussed by Levy and Levy.
Part III presents contributions on the surprising tolerance and diversity of
eukaryotes to hypoxia and anoxia, demonstrating that anoxic life is not strictly
anaerobic microbes able to cope with the reducing chemical habitat of their substrate.
All kinds of biota may attune to anoxic conditions following the demands of
xii
STEPPING INTO THE BOOK OF ANOXIA AND EUKARYOTES
hosted symbionts, for prolonging the survival and success of their offspring and
encystments, for enhancement of their competitiveness, and/or for successful
survival and rapid repopulation after sporadic oxygen defi ciency. Very different
eukaryotes employ considerable and sometimes decisive advantage by coping and
managing anoxic conditions; and all this for quite varied reasons. These chapters
cover magnetotactic protists (Bazylinski et al.), ciliates (Beaudoin et al.), and

protistan symbionts hosted by termites (Dolan). In addition, a number of experi-
mental works involve insects (Hoback), brine shrimp (Clegg), and the superstar
specialists in surviving super-stressors, the tardigrades (Horikawa). Even fl owering
plants face driving forces to acquire specifi c capabilities for coping with pulsed or
sporadic anoxia (Crawford).
A specialized part of the book, Part IV, presents work on Foraminifera,
which are a unique taxon in that most extant forms easily fossilize (vs. metazoans
and other protists common to anoxic habitats) and because foraminifera have
been shown to perform complete denitrifi cation (Koho and Pina-Ochoa). Thus,
this group could be considered a key taxon with respect to facultative eukaryotic
anaerobiosis (Heinz and Geslin). Distribution-oriented studies (Mallon et al.;
Cardich et al.) illustrate how abundant this group can be in certain oxygen-
depleted settings.
Part V focuses on community responses in specifi c oxygen-stressed habitats.
Our planet faces increasing surface temperatures, record-breaking heat in summers,
catastrophic storms and rain falls, and the most rapid melting of ice sheets and
mountain glaciers ever observed by humans. Declining densities of surface waters
reduce mixing rates with deeper water masses, the intensity of downwelling, and
the supply of well-oxygenated bottom water masses. Increased surface water
temperatures as well as the enhanced infl ow of freshwater from melting ice shields
cause such density drops. Marine realms with enhanced degradation of organic
carbon fl uxes and oxygen consumption, called oxygen minimum zones (OMZ),
seem highly sensitive to these perturbations. These regions are actively becoming
more and more depleted in oxygen. Their annual reduction of dissolved oxygen
ranges from about 0.1 to 0.4 μmol per liter of seawater at mid-water depths,
expanding the area where larger metazoa start to suffer from hypoxia by 4.5
million km
2
during the last decades (see Stramma et al. 2010 in Table 1 ). As the inner
core of such OMZ’s may reach anoxia, the expansion of ocean-wide “death zones”

is forewarned (Gewin 2010, Table 1 ), with hypoxia and anoxia as prime stressors
(Buck et al.). Inevitably, hypoxia and anoxia must be monitored more carefully in
the future, in order to follow environmental change (Stachowitsch et al.). Well-
investigated hypoxic to anoxic regions, such as the Black Sea (Sergeeva et al.),
stratifi ed basins (Sacca), silled fjord basins (Stoecke and Behnke), and meromictic
lakes (Fritz et al.) still offer new insights about community responses after close
examination. More recently, chemolithotrophic groundwaters (Por) and the deep
sedimentary habitats (Edgcomb and Biddle) have started to attract a growing
number of scientists, and are expected to deliver a wealth of new insights, novel
biota, and fascinating biogeochemical dynamics.
xiii
STEPPING INTO THE BOOK OF ANOXIA AND EUKARYOTES
Table 1. Thresholds, ranges, and technical terms in use for the definition of dissolved oxygen concen-
trations, their biotic response, and observed environmental impacts and repercussions.
Range ª m mol/kg Term Indication Reference
>8–2 ml/l 400–100 Oxic Geochemists relate this term
primarily to redox conditions (Eh),
biologists to availability of O
2

Tyson and Pearson
(1991)
2–0.2 ml/l 100–10 Dysoxic Seasonal dysoxic conditions occur
in stratified estuarine or pro-delta
settings, more extensively on open
shelves at water depths deeper
than 60 m, and in near bottom
water
Tyson and Pearson
(1991)

120–60 m mol/kg 120–60 Hypoxic Lethal or stressful to specific
mobile macro-organisms
Stramma et al. (2008)
<70 m mol/kg 70 Some large mobile macro-
organisms are unable to abide
Stramma et al. (2010)
<2 mg/l 70 Reduction of meiofaunal
abundance and diversity
Wetzel et al. (2001)
<1.5 ml/l 68 Critical for larger fish Gewin (2010)
<63 m mol 63 Range for the definition of spe-
cific biotic and biogeo chemical
consequences of coastal
“hypoxia”
Helly and Levin (2004),
Middelburg and Levin
(2009)
1.42 ml/l 62.5 Threshold for coastal seafloor
hypoxia, near 30% oxygen
saturation
Levin et al. (2009)
<5 kPa O
2
50 Onset for specific physiological
adaptations required for certain
transition of ecosystems
Seibel (2011)
>1 ml/l 45 Oxic Technical term Bernhard and Sen
Gupta (1999), Levin
(2004)

1–0.1 ml/l 45–4.5 Dysoxic Technical term Bernhard and Sen
Gupta (1999),
Levin (2004)
<0.5 ml/l 22 Threshold for contour lining
“hypoxic” oxygen depletion on
shelves and bathyal sea floors
Helly and Levin (2004)
20 m mol 20 Suboxia Upper threshold of the transition
layer from O
2
to NO
3

−
respiration,
(0.7–20 m mol), termed “suboxia”
by biologists and biogeochemists
Helly and Levin (2004),
Middelburg
and Levin (2009)
<20 m mol 20 Global definition of the most
intense oxygen minimum zones
(OMZ)
Helly and Levin (2004),
Middelburg
and Levin (2009)
<1 kPa O
2
10 Threshold for a certain transition
of ecosystems; represents a limit

to evolved oxygen extraction
capacity
Seibel (2011)
(continued)
xiv
STEPPING INTO THE BOOK OF ANOXIA AND EUKARYOTES
Range ª m mol/kg Term Indication Reference
0.2–0.0 ml/l 10 Suboxic Formation of laminated
sediments without macrofauna,
but with in situ microfauna
Tyson and Pearson
(1991)
<10 m mol/kg 10 Suboxic Nitrate becomes involved
in respiration if present
Stramma et al. (2008)
<0.15 ml/l 10 Bioturbation is reduced,
chemosynthesis becomes important
Levin (2004)
<10 m M 10 Accuracy of common O
2
probes
in field research
Paulmier and
Ruiz-Pino (2009)
10–2 m M 10–2 Reproducibility of O
2
measures
in the field
Paulmier and
Ruiz-Pino (2009)

>0.2 ml/l 9 No effect on midwater biomass,
low effect on biodiversity
Childress and Seibel
(1998)
<0.2 ml/l 9 Threshold for contour lining a
more strict definition of “hypoxia”
Helly and Levin (2004)
<0.15 ml/l 7 Significant drop in zooplankton
biomass
Childress and Seibel
(1998)
2–6 m mol/l 2–6 C – layer Coexistence of H
2
S and O
2
Sorokin (2005)
<0.1 ml/l 4.5 Suboxic Marks a distinct change in the
environment, rise of nitrate removal
Karstensen et al. (2008)
>0–0.1 ml/l 4.5 Microxic Technical term Bernhard and Sen
Gupta (1999),
Levin (2004)
m 50 Ciliate 2–4 Half-saturation for larger ciliates
( » 1–2% atm. pressure)
Fenchel and Finlay
(2008)
>10
−6
mol 1 Accuracy of high level O
2

detection methodologies
(< » 0.5% saturation)
Berner (1981), Paulmier
and Ruiz-Pino (2009)
1 m mol 1 Minimum level reached in the
core of OMZs
Helly and Levin (2004),
Middelburg and Levin
(2009)
0.7 m mol 0.7 Suboxia Lower threshold of the transition
layer from O
2
to NO
3

−
respiration
(0.7–20 m mol/kg)
Helly and Levin (2004),
Middelburg and Levin
(2009)
m 50 Amoeba 0.4 Half-saturation for an amoeba
( » 0.2% of atmospheric pressure)
Fenchel and Finlay
(2008)
m 50 Yeast 0.15 Half-saturation for yeast cells
( » 0.07% of atmospheric pressure)
Fenchel and Finlay
(2008)

m 50 Bacteria 0.1 Half-saturation for bacteria
and mitochondria ( » 0.05%
of atmospheric pressure)
Fenchel and Finlay
(2008)
0 ml/l 0 Postoxic Neither free oxygen nor reducing
conditions (e.g., production of
hydrogen sulfide)
Berner (1981),
Baernhard and Sen
Gupta (1999)
0 ml/l 0 Anoxic No dissolved oxygen Baernhard and Sen
Gupta (1999), Levin
(2004), Stramma et al.
(2008), and Tyson and
Pearson (1991)
Table 1. (continued)
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STEPPING INTO THE BOOK OF ANOXIA AND EUKARYOTES
Part VI turns back in time in search for signals, tracers and evidence from
modern anoxic environments that can be applied to the reconstruction, and
understanding of the fossil record. Stable isotopes are commonly used in biogeo-
chemistry, but rarely scaled for their specifi c behavior under anoxia (Struck;
Altenbach et al.). Test porosity in Foraminifera channels diffusional gradients
between the cell and the environment. New insights indicate that nitrate utilization
and denitrifi cation might be deduced using modern and fossil test porosity (Glock
et al.). Also, the correlation between modern and Mesozoic upwelling systems is
discussed (Almogi et al.), as are analogs of foraminiferal test structures in
Devonian black shales and modern Foraminifera from the Santa Barbara Basin
(Schieber). Many recent insights into modern facultative anaerobic Foraminifera

support a hypothesis on the basic reasons for foraminiferal test construction
(Altenbach and Gaulke), and even more far-reaching speculations about the
evolutionary path in these rhizarians (Altermann et al.).
Common terms in use for distinguishing levels of oxygen defi ciency in envi-
ronments, for biota, in physiology, in clinical research, and in geosciences may be
identical, but their defi nitions may be quite variable in different disciplines of
natural sciences. The terms “hypoxia” and “hypoxic” are basically clinical termi-
nologies that defi ne a pathological condition of an organism or its tissues when
deprived of appropriate oxygen availability, as opposed to stress-free “normoxia”
or “normoxic” conditions. However, these terms are meanwhile broadly used in
environmental research, indicating depleted oxygen conditions irrespective of
stress impact on biota. But as hypoxia might be reached for different biota at very
different oxygen concentrations, this term should not be linked to an explicit
level or range of dissolved oxygen available in the environment. In physiology, the
half-saturation constant “μ50” is a common measure. It marks the substrate
concentration at which “μ” equals half of the maximum rate of growth/turnover/
consumption “μmax” of an organism or a cellular structure. The term “euxinia”
was coined by considerations on sedimentary facies in geosciences; it defi nes
either stagnant water exchange or reduced solubility of oxygen, provoking oxygen
depletion down to anoxia rather than a specifi c level of dissolved oxygen.
Sedimentologists often condense confl icting redox conditions to the recon-
struction of either “euxinic” conditions, which means that sulfi de was present and
molecular oxygen practically absent in the water column, or they consider “suboxic”
conditions, which defi nes residual molecular oxygen in the bottom water but also
sulfi de production within or at the surface of the sediment column.
Table 1 provides a guide for the different units, ranges, and terms used in this
book and an e
xample of the wide range of literature employing them. The fi rst
column quotes the threshold or range exemplifi ed in a source reference quoted in
column fi ve. The second column unifi es this unit to μmol, either as given in the

respective source or roughly calculated without specifi c corrections (e.g., for
temperature, density, media, etc.). The third column refers to the specifi c terminology
in use, and the fourth column describes its basic usage.
xvi
STEPPING INTO THE BOOK OF ANOXIA AND EUKARYOTES
Last but not the least, it may be noted that the defi nition of “anoxia” itself – as
complete absence of dissolved oxygen – is easily defi ned, but impossible to measure
in the fi eld. Most fi eld methodologies available are not able to detect concentrations
below 1 μmol, and their reproducibility may range well above 2 μmol (Table 1 ).
This r
ange of methodological restriction can interfere with a number low level
thresholds presented in Table 1 . When approaching anoxia, methods must
necessarily be more and more sophisticated. In addition, Eh profi ling and specifi c
biochemical analyses should extend oxygen probe measures. Fine-tuning between
suboxic, postoxic, and anoxic conditions is a meticulous task under debate
(see Sorokin 2007). However, whether chemically aggressive, free radicals are
present or not may be more decisive for the prevailing eukaryotes than small-scale
drops in O
2
concentrations already near zero. For a multitude of research topics,
there is much future work to defi ne what anoxia is, and what eukaryotes actually
do during exposure to anoxia. We hope many readers of this book will dedicate
studies to these unknowns.
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xvii
STEPPING INTO THE BOOK OF ANOXIA AND EUKARYOTES
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biological impacts. Deep Sea Res I 57:587–595
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Alexander V. Altenbach, Joan M. Bernhard, and Joseph Seckbach
The Editors. Munich, Woods Hole, Jerusalem

xix
Biodata of Alexander V . Altenbach , Joan M . Bernhard, and Joseph Seckbach , the
editors of this volume.
Dr. Alexander Volker Altenbach earned his Ph.D. from Kiel University in 1985,
followed by activities as a reader, team leader, and chief scientists in paleoceano-
graphy and micropaleontology in Kiel. Cooperation with multidisciplinary joint
research units and the Geomar Research Center convinced him that mainly inter-
disciplinary geobiochemical approaches pave the way for understanding system
earth. External affairs sum up from mudlogging and engineering geology to
cofounding a software company in Hamburg.
Since 1994, he is Professor for micropaleontology at the Dept. of Earth and
Environmental Science of the Ludwig-Maximilians-University in Munich
(Germany). Times in Munich include activities as Chaperon of the Bavarian
States Collection for Micropaleontology, Speaker of the Research Center for
Geobiology and Biodiversity, and Dean of the Faculty of Geosciences.
All in all, years were spent on research vessels, boats, scuba diving, and during
fi eld excursions on fi ve oceans and continents, among them very fruitful sabbaticals
at the Australian National University in Canberra, and at the Huinay Research
Station in Patagonia. Publications mainly deal with Foraminifera, but some do
also cover the development of laboratory equipment and software, tectonics,
fossils, the ecology of lizards and snakes, and a natural fi eld guide to Australia.
Most investigations center on ecology, biomass, food webs, and stable isotope
fractionation.
Reasonable for getting involved in this book was the rejection of an early
manuscript on foraminifera thriving under sulfi dic conditions by two internationally

recommended journals. As noted by a critical reviewer, this was because “anoxic
foraminifera don’t seem reasonable.”
E-mail:
xx
Dr. Joan M . Bernhard , who is a Senior Scientist at Woods Hole Oceanographic
Institution (Massachusetts, USA), is a biogeochemist with a major focus on the
adaptations and ecology of protists living in the chemocline. Another focus of her
work uses experimental approaches to investigate the controls on geochemical
proxies recorded in calcareous foraminiferal tests (shells), as well as other aspects
of foraminiferal biology. Her work largely involves the bathyal to abyssal deep sea
and recently has concentrated on modern environments and organisms, but her
career began with interpretation of the fossil record. She continues to do paleoe-
cologically and paleoceanographically relevant research.
Bernhard has degrees in geology (B.A. 1982, Colgate University; M.S. 1984,
University of California Davis) and biological oceanography (Ph.D. 1990, Scripps
Institution of Oceanography, University of California San Diego), and did post-
doctoral work in cell biology at the Wadsworth Center (New York State
Department of Health, Albany New York). She also worked in the Department
of Environmental Health Sciences at the University of South Carolina’s Arnold
School of Public Health from 1997 to 2004. She has served as Chief Scientist on
18 research cruises and participant on 33 others. Her research has included
submersible and Remotely Operated Vehicle (ROV) work. Her earlier career
included nine fi eld seasons totaling 23 months in the Antarctic, performing nearly
200 SCUBA dives under ice.
Her multidisciplinary training and diverse experience gives her a unique
perspective into anoxic habitats.
E-mail:
xxi
Biodata of Joseph Seckbach , editor of this volume, and author of “ Introduction
to Anoxia : Evidence for Eukaryote Survival and Paleontological Strategies”.

Professor Joseph Seckbach is the founder and chief editor of Cellular Origins ,
Life in Extreme Habitats and Astrobiology (“COLE”) book series (the present
volume is number 21 of this series, see: www.springer.com/series/5775 ). He has
coedited other v
olumes, such as the Proceeding of Endocytobiology VII
Conference (Freiburg, Germany) and the Proceedings of Algae and Extreme
Environments Meeting (Trebon, Czech Republic). See weizerbart.
de/pubs/books/bo/novahedwig-051012300-desc.ht ). His recent volume (with coeditor
Richard Gordon) entitled Divine Action and Natural Selection: Science, Faith,
and Evolution was published by World Scientifi c Publishing Company.
Dr. Seckbach earned his Ph.D. from the University of Chicago (1965) and
did a postdoctoral training in the Division of Biology at Caltech, in Pasadena,
CA. He was appointed to the faculty of the Hebrew University (Jerusalem,
Israel). He spent sabbaticals at UCLA and Harvard University and DAAD-
sponsored periods in Tübingen, Germany, and at LMU, Munich. Dr. Seckbach
served at Louisiana State University, Baton Rouge, as the fi rst selected occupant
of the Endowed Chair for the Louisiana Sea Grant and Technology transfer.
Beyond editing academic volumes, he has published scientifi c articles on
plant ferritin–phytoferritin, cellular evolution, acidothermophilic algae, and life
in extreme environments. He also edited and translated several popular books.
Professor Seckbach is the coauthor, with R. Ikan, of the Hebrew language
Chemistry Lexicon (DeVeer publisher, Tel Aviv, Israel). His recent interest is in the
fi eld of enigmatic microorganisms and life in extreme environments.
E-mail:

xxiii
LIST OF AUTHORS AND THEIR ADDRESSES
ALMOGI-LABIN, AHUVA
GEOLOGICAL SURVEY OF ISRAEL, 30 MALKHE ISRAEL ST.,
JERUSALEM 95501, ISRAEL

ALTENBACH, ALEXANDER VOLKER
DEPARTMENT FOR EARTH AND ENVIRONMENTAL SCIENCE ,
AND GEOBIO-CENTER, LUDWIG-MAXIMILIANS-UNIVERSITÄT,
MUNICH, AND RICHARD-WAGNER-STR. 10, 80333 MUNICH,
GERMANY
ALTERMANN, WLADYSLAW
DEPARTMENT OF GEOLOGY, UNIVERSITY OF PRETORIA,
PRETORIA 0002, SOUTH AFRICA
ANIKEEVA, OKSANA V.
INSTITUTE OF BIOLOGY OF THE SOUTHERN SEAS NASU ,
SEVASTOPOL, UKRAINE
ASHCKENAZI-POLIVODA, SARIT
GEOLOGICAL SURVEY OF ISRAEL , 30 MALKHE ISRAEL ST.,
JERUSALEM 95501, ISRAEL
DEPARTMENT OF GEOLOGICAL AND ENVIRONMENTAL SCIENCES ,
BEN GURION UNIVERSITY OF THE NEGEV , BEER SHEVA 84105,
ISRAEL
BARRY, JAMES P.
MONTEREY BAY AQUARIUM RESEARCH INSTITUTE,
7700 SANDHOLDT ROAD, MOSS LANDING , CA 95039, USA
BAZYLINSKI, DENNIS A.
SCHOOL OF LIFE SCIENCES , UNIVERSITY OF NEVADA AT LAS VEGAS ,
4505 MARYLAND PARKWAY , LAS VEGAS , NV 89154-4004, USA
BEAUDOIN, DAVID J.
BIOLOGY DEPARTMENT , WOODS HOLE OCEANOGRAPHIC
INSTITUTION , WOODS HOLE , MA 02543 , USA
xxiv
LIST OF AUTHORS AND THEIR ADDRESSES
BEHNKE, ANKE
DEPARTMENT OF ECOLOGY , UNIVERSITY OF KAISERSLAUTERN ,

ERWIN SCHROEDINGER STR. 14 , KAISERSLAUTERN D-67663 ,
GERMANY
BENJAMINI, CHAIM
DEPARTMENT OF GEOLOGICAL AND ENVIRONMENTAL SCIENCES ,
BEN GURION UNIVERSITY OF THE NEGEV , BEER SHEVA 84105,
ISRAEL
RAMON SCIENCE CENTER, MIZPE RAMON 80600, ISRAEL
BERNHARD, JOAN M.
GEOLOGY AND GEOPHYSICS DEPARTMENT , WOODS HOLE
OCEANOGRAPHIC INSTITUTION , MS #52 , WOODS HOLE ,
MA 02543, USA
BIDDLE, JENNIFER F.
COLLEGE OF EARTH, OCEAN AND THE ENVIRONMENT ,
UNIVERSITY OF DELAWARE , LEWES , DE 19958, USA
BRÜMMER, FRANZ
DEPARTMENT OF ZOOLOGY, BIOLOGICAL INSTITUTE ,
UNIVERSITY OF STUTTGART , 70569 STUTTGART, GERMANY
BUCK, KURT R.
MONTEREY BAY AQUARIUM RESEARCH INSTITUTE , 7700
SANDHOLDT ROAD , MOSS LANDING , CA 95039 , USA
CARDICH, JORGE
FACULTAD DE CIENCIAS Y FILOSOFÍA, PROGRAMA MAESTRÍA
EN CIENCIAS DEL MAR , UNIVERSIDAD PERUANA CAYETANO
HEREDIA , AV. HONORIO DELGADO 430 , LIMA 31, PERU
DIRECCIÓN DE INVESTIGACIONES OCEANOGRÁFICAS ,
INSTITUTO DEL, MAR DEL PERÚ (IMARPE), AV. GAMARRA Y
GRAL. VALLE, S/N, CHUCUITO , CALLAO , PERU
JOINT INTERNATIONAL LABORATORY ‘DYNAMICS OF THE
HUMBOLDT CURRENT SYSTEM’ (LMI DISCOH), LIMA, PERU
CLEGG, JAMES S.

BODEGA MARINE, LABORATORY, SECTION OF MOLECULAR
AND CELLULAR BIOLOGY , UNIVERSITY OF CALIFORNIA , DAVIS,
BODEGA BAY , CA 94923, USA