Anoxia Evidence for Eukaryote Survival and Paleontological Strategies pdf

287The Response of Benthic Foraminifera to Low-Oxygen Conditions of the Peruvian Oxygen Minimum Zone [Mallon, J.. Anaerobic areas of marine or fresh water that are depleted of dissolved

Volume 21

Series Editor:

Joseph Seckbach

The Hebrew University of Jerusalem, Israel

For further volumes:

http://www.springer.com/series/5775

Alexander V Altenbach

Department for Earth and Environmental

Science, and GeoBio-Center

jbernhard@whoi.edu

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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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

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.] 145The Wood-Eating Termite Hindgut: Diverse Cellular

Symbioses in a Microoxic to Anoxic Environment

[Dolan, M.F.] 155Ecological and Experimental Exposure of Insects to Anoxia

Reveals Surprising Tolerance [Hoback, W.W.] 167The Unusual Response of Encysted Embryos of the Animal

Extremophile, Artemia franciscana, to Prolonged Anoxia

[Clegg, J.S.] 189Survival 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.] 249Ecological and Biological Response of Benthic Foraminifera

Under Oxygen-Depleted Conditions: Evidence from

Laboratory Approaches [Heinz, P and Geslin, E.] 287The Response of Benthic Foraminifera to Low-Oxygen Conditions

of the Peruvian Oxygen Minimum Zone

[Mallon, J et al.] 305Benthic 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

The Return of Shallow Shelf Seas as Extreme Environments:

Anoxia and Macrofauna Reactions in the Northern

Adriatic Sea [Stachowitsch, M et al.] 353Meiobenthos of the Oxic/Anoxic Interface in the Southwestern

Region of the Black Sea: Abundance and Taxonomic

Composition [Sergeeva, N.G et al.] 369The Role of Eukaryotes in the Anaerobic Food Web

of Stratifi ed Lakes [Saccà, A.] 403The Anoxic Framvaren Fjord as a Model System to Study

Protistan Diversity and Evolution

[Stoeck, T and Behnke, A.] 421Characterizing 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.] 463Microbial 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.] 515The Functionality of Pores in Benthic Foraminifera

in View of Bottom Water Oxygenation: A Review

[Glock, N et al.] 537Anoxia-Dysoxia at the Sediment-Water Interface of the Southern

Tethys in the Late Cretaceous: Mishash Formation,

Southern Israel [Almogi-Labin, A et al.] 553Styles 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.] 573Did Redox Conditions Trigger Test Templates in Proterozoic

Foraminifera? [Altenbach, A.V and Gaulke, M.] 591The Relevance of Anoxic and Agglutinated Benthic Foraminifera

to the Possible Archean Evolution of Eukaryotes

[Altermann, W et al.] 615

Organism Index 631Subject Index 639Author Index 647

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

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 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

contri-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

Jerusalem, Israel

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 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

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

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)

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

Gupta (1999), Levin (2004)

m 50 Ciliate 2–4 Half-saturation for larger ciliates

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)

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)

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 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”

envi-or “nenvi-ormoxic” 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 example 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

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 range 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

References

Berner RA (1981) A new geochemical classifi cation of sedimentary environments J Sed Petrol 51:359–365 Bernhard JM, Sen Gupta B (1999) Foraminifera of oxygen-depleted environments In: Sen Gupta B (ed) Modern Foraminifera Kluwer Academic, Dordrecht, pp 200–216

Childress JJ, Seibel BA (1998) Life at stable low oxygen levels: adaptations of animals to oceanic oxygen minimum layers J Exp Biol 201:1223–1232

Fenchel T, Finlay B (2008) Oxygen and the spatial structure of microbial communities Biol Rev 83:553–569

Gewin V (2010) Dead in the water Nature, 466:812–814

Helly JJ, Levin LA (2004) Global distribution of naturally occurring marine hypoxia on continental margins Deep-Sea Res I 51:1159–1168

Karstensen J, Stramma L, Visbeck M (2008) Oxygen minimum zones in the eastern tropical Atlantic and Pacifi c oceans Prog Oceanogr 77:331–350

Levin LA (2004) Oxygen minimum zone benthos: adaptation and community response to hypoxia In: Gibson RN, Atkinson RJA (ed) Oceanography and marine biology, an annual review, vol 41 CRC Press, Boca Raton, pp 1–45

Levin LA, Ekau W, Gooday AJ, Jorissen F, Middelburg JJ, Naqvi SWA, Neira C, Rabalais NN, Zhang J (2009) Effects of natural and human-induced hypoxia on coastal benthos Biogeo- sciences 6:2063–2098

Middelburg JJ, Levin LA (2009) Coastal hypoxia and sediment biogeochemistry Biogeosciences 6:1273–1293

Paulmier A, Ruiz-Pino D (2009) Oxygen minimum Zones (OMZs) in the modern ocean Prog Oceanogr 80:113–128

Seibel BA (2011) Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones

Stramma L, Schmidtko S, Levin LA, Johnson GC (2010) Ocean oxygen minima expansions and their biological impacts Deep Sea Res I 57:587–595

Tyson RV, Pearson TH (1991) Modern and ancient continental shelf anoxia: an overview Geol Soc Lond Spec Publ 58:1–24

Wetzel MA, Fleeger JW, Powers SP (2001) Effects of hypoxia and anoxia on meiofauna: a review with new data from the Gulf of Mexico Coast Est Stud 58:165–184

Alexander V Altenbach, Joan M Bernhard, and Joseph Seckbach

The Editors Munich, Woods Hole, Jerusalem

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 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: a.altenbach@lrz.uni-muenchen.de

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: jbernhard@whoi.edu

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: seckbach@huji.ac.il

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

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

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

CRAWFORD, ROBERT M M

SCHOOL OF BIOLOGY , THE UNIVERSITY OF ST ANDREWS ,

ST ANDREWS KY16 AL , SCOTLAND, UK

DE GRAAF, ROB M

DEPARTMENT OF EVOLUTIONARY MICROBIOLOGY, FACULTY

OF SCIENCE , RADBOUD UNIVERSITY NIJMEGEN ,

HEYENDAALSEWEG 135 , 6525AJ NIJMEGEN, THE NETHERLANDS

GEOLOGY AND GEOPHYSICS DEPARTMENT , WOODS HOLE

OCEANOGRAPHIC INSTITUTION , WOODS HOLE, MA 02543 , USA

DEPARTMENT OF ZOOLOGY, BIOLOGICAL INSTITUTE ,

UNIVERSITY OF STUTTGART , 70569 STUTTGART, GERMANY

GAULKE, MAREN

GEOBIO-CENTER , LUDWIG-MAXIMILIANS-UNIVERSITY , WAGNER-STR 10 , 80333 MUNICH, GERMANY

GESLIN, EMMANUELLE

LABORATOIRE D`ETUDE DES BIO-INDICATEURS ACTUELS

ET FOSSILES (BIAF) AND LEBIM , UNIVERSITY OF ANGERS ,

2 BOULEVARD LAVOISIER , ANGERS CEDEX 49045, FRANCE

GLOCK, NICOLAAS

CHRISTIAN-ALBRECHTS-UNIVERSITY KIEL ,

SONDERFORSCHUNGSBEREICH 754 , KIEL , GERMANY

LEIBNIZ INSTITUTE OF MARINE SCIENCES,

IFM-GEOMAR , WISCHHOFSTRASSE 1-3 , D-24148 KIEL , GERMANY

GOODAY, ANDREW J

NATIONAL OCEANOGRAPHY CENTRE , SOUTHAMPTON SO14 3ZH , UK

GUTIÉRREZ, DIMITRI

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

HACKSTEIN, JOHANNES H P

DEPARTMENT OF EVOLUTIONARY MICROBIOLOGY, FACULTY

OF SCIENCE , RADBOUD UNIVERSITY NIJMEGEN ,

HEYENDAALSEWEG 135 , 6525AJ NIJMEGEN , THE NETHERLANDS

HEINZ, PETRA

DEPARTMENT FOR GEOSCIENCES , UNIVERSITY OF TÜBINGEN , HÖLDERLINSTR 12 , TÜBINGEN 72074 , GERMANY

HENGHERR, STEFFEN

DEPARTMENT OF ZOOLOGY, BIOLOGICAL INSTITUTE ,

UNIVERSITY OF STUTTGART , 70569 STUTTGART , GERMANY

HISS, MARTIN

GEOLOGICAL SURVEY NRW , 1080, 47710 KREFELD , GERMANY

HOBACK, WILLIAM WYATT

DEPARTMENT OF BIOLOGY , UNIVERSITY OF NEBRASKA

AT KEARNEY , 905 WEST 25TH STREET , KEARNEY 68849, NE , USA

HORIKAWA, DAIKI D

UNIVERSETY PARIS DESCARTES-SITE NECKER, INSERM U 1001 ,

75751, PARIS CEDEX 15 , FRANCE

MEDITERRANEAN INSTITUTE FOR LIFE SCIENCES , 21000 SPLIT , CROATIA

KOHO, KAROLIINA A

DEPARTMENT OF EARTH SCIENCES, FACULTY

OF GEOSCIENCES , UTRECHT UNIVERSITY , BUDAPESTLAAN 4 ,

3584 CD UTRECHT , THE NETHERLANDS

SCHOOL OF LIFE SCIENCES , UNIVERSITY OF NEVADA

AT LAS VEGAS , 4505 MARYLAND PARKWAY , LAS VEGAS, NV

89154-4004 , USA

LEGER, MICHELLE M

DEPARTMENT OF BIOCHEMISTRY AND MOLECULAR BIOLOGY, CENTRE FOR COMPARATIVE GENOMICS AND EVOLUTIONARY BIOINFORMATICS , DALHOUSIE UNIVERSITY , HALIFAX , CANADA B3H 4R2

LEITER, CAROLA

DEPARTMENT FOR EARTH AND ENVIRONMENTAL SCIENCE , LMU MUNICH , RICHARD-WAGNER-STR 10 , 80333 MUNICH , GERMANY GEOBIOCENTER LUDWIG-MAXIMILIANS-UNIVERSITY ,

RICHARD-WAGNER-STR 10 , 80333 MUNICH , GERMANY

MALLON, JÜRGEN

CHRISTIAN-ALBRECHTS-UNIVERSITY KIEL ,

SONDERFORSCHUNGSBEREICH 754 , KIEL , GERMANY

LEIBNIZ INSTITUTE OF MARINE SCIENCES,

IFM-GEOMAR , WISCHHOFSTRASSE 1-3, D-24148 KIEL , GERMANY

MAYR, CHRISTOPH

GEOBIO-CENTERLMU , RICHARD-WAGNER-STR 10 , 80333 MUNICH , GERMANY AND INSTITUTE FOR GEOGRAPHY , FAU NÜRNBERG/ERLANGEN , KOCHSTR 4/4 , 91054 ERLANGEN , GERMANY

MAZLUMYAN, SOFIA A

INSTITUTE OF BIOLOGY OF THE SOUTHERN SEAS NASU ,

SEVASTOPOL , UKRAINE

MORALES, MARÍA

LABORATORIO DE MICROPALEONTOLOGÍA , INSTITUTO

GEOLÓGICO MINERO METALÚRGICO (INGEMMET) , AV CANADÁ

1470 , LIMA 41 , PERU

OREN, AHARON

DEPARTMENT OF PLANT AND ENVIRONMENTAL SCIENCES,

THE INSTITUTE OF LIFE SCIENCES, AND THE MOSHE SHILO

MINERVA CENTER FOR MARINE BIOGEOCHEMISTRY , THE

HEBREW UNIVERSITY OF JERUSALEM , 91904 JERUSALEM , ISRAEL

PIÑA-OCHOA, ELISA

CENTER FOR GEOMICROBIOLOGY, INSTITUTE OF BIOLOGICAL SCIENCES , AARHUS UNIVERSITY , DK-8000 AARHUS , DENMARK

PFANNKUCHEN, MARTIN

RUÐER BOŠKOVIŠ INSTITUTE , ROVINJ , CROATIA

POR, FRANCIS DOV

DEPARTMENT OF EVOLUTION, ECOLOGY AND BEHAVIOUR,

NATIONAL COLLECTIONS OF NATURAL HISTORY , THE HEBREW UNIVERSITY OF JERUSALEM , GIVAT RAM , 91904 JERUSALEM ,

ISRAEL

QUIPÚZCOA, LUIS

DIRECCIÓN DE INVESTIGACIONES OCEANOGRÁFICAS , INSTITUTO DEL, MAR DEL PERÚ (IMARPE) , AV GAMARRA Y GRAL VALLE, S/N, CHUCUITO , CALLAO , PERU

LEIBNIZ INSTITUTE OF MARINE SCIENCES,

IFM-GEOMAR , WISCHHOFSTRASSE 1-3 , D-24148 KIEL , GERMANY

DEPARTMENT OF ZOOLOGY, BIOLOGICAL INSTITUTE,

UNIVERSITY OF STUTTGART, 70569 STUTTGART , GERMANY

TREUDE, TINA

DEPARTMENT OF MARINE BIOGEOCHEMISTRY, LEIBNIZ

INSTITUTE OF MARINE SCIENCES (IFM-GEOMAR), 24148 KIEL , GERMANY

TSAOUSIS, ANASTASIOS D

DEPARTMENT OF BIOCHEMISTRY AND MOLECULAR BIOLOGY, CENTRE FOR COMPARATIVE GENOMICS AND EVOLUTIONARY BIOINFORMATICS , DALHOUSIE UNIVERSITY , HALIFAX , CANADA B3H B3H 4R2

ZUSCHIN, MARTIN

DEPARTMENT OF PALEONTOLOGY , UNIVERSITY OF VIENNA , ALTHANSTRASSE 14 , 1090 VIENNA , AUSTRIA

BARNHART, MILES CHRISTOPHER

DEPARTMENT OF BIOLOGY, MISSOURI STATE UNIVERSITY,

DEPARTMENT OF BIOLOGY, CHADRON STATE COLLEGE,

1000 MAIN STREET, CHADRON, NE 69337, 308-432-6446, USA

BUNGE, JOHN A

DEPT STATISTICAL SCIENCES, CORNELL UNIVERSITY,

COMSTOCK HALL-ACADEMIC II, ROOM 1198, ITHACA, USA

DE TULLIO, MARIO C

DIPART DI BIOLOGIA E PATOLOGIA VEGETALE,

UNIVERSITÀ DI BARI, VIA E, ORABONA 4, BARI, I-70125, ITALY

DYER, BETSEY D

WHEATON COLLEGE, 26 EAST MAIN STREET, NORTON,

MA 02766–2322, USA

FRENZEL, PETER

FRIEDRICH SCHILLER UNIVERSITY OF JENA, INSTITUTE

OF EARTH SCIENCES, BURGWEG 11, D-07749 JENA, GERMANY

VAN DER GIEZEN, MARK

CENTRE FOR EUKARYOTIC EVOLUTIONARY MICROBIOLOGY,

COLLEGE OF LIFE AND ENVIRONMENTAL SCIENCES,

UNIVERSITY OF EXETER, STOCKER ROAD, EXETER, EX4 4QD, UNITED KINGDOM

HASEMANN, CHRISTIANE

DEEP SEA ECOLOGY AND TECHNOLOGY, ALFRED WEGENER INSTITUTE, AM HANDELSHAFEN 12, D-27570, BREMERHAVEN, GERMANY

KORMAS, KONSTANTINOS AR

AQUATIC MICROBIAL ECOLOGY, DEPARTMENT OF

ICHTHYOLOGY & AQUATIC ENVIRONMENT, UNIVERSITY

OF THESSALY, 384 46 NEA IONIA, GREECE

KUHNT, WOLFGANG

MARINE MICROPALEONTOLOGY,

CHRISTINA-ALBERTINA-UNIVERSITY, LUDEWIG-MEYN-STR 14, D-24118 KIEL, GERMANY

LEADBETTER, JARED

CALIFORNIA INSTITUTE OF TECHNOLOGY, ENVIRONMENTAL SCIENCE & ENGINEERING, 137 KECK LABORATORIES, MAILCODE 138–78, PASADENA, CA 91125–7800, USA

LOPEZ-GARCIA, PURIFICATION

UNITÉ D’ECOLOGIE, SYSTÉMATIQUE ET EVOLUTION, UMR CNRS

8079, BÂTIMENT 360, UNIVERSITE PARIS-SUD, 91405 ORSAY CEDEX, FRANCE

MCLENNAN, ALEXANDER

INSTITUTE OF INTEGRATIVE BIOLOGY, CELL REGULATION AND SIGNALLING DIVISION, UNIVERSITY OF LIVERPOOL, LIVERPOOL L69 7ZB, UNITED KINGDOM

MEYSMAN, FILIP

NETHERLANDS INSTITUTE OF ECOLOGY, CENTRE FOR

ESTUARINE AND MARINE ECOLOGY, KORRINGAWEG 7,

4401 NT YERSEKE, THE NETHERLANDS

NIELSEN, LARS PETER

DEPT OF BIOLOGICAL SCIENCES, AARHUS UNIVERSITY,

BYNING 1540, NY MUNKEGADE 116, 8000 ARHUS, DENMARK

PAWLOWSKI, JAN

DEPT OF ZOOLOGY AND ANIMAL BIOLOGY, UNIVERSITY

OF GENEVA, CH-1211 GENEVA 4, SWITZERLAND

POLLEHNE, FALK

BIOLOGICAL OCEANOGRAPHY, LEIBNIZ INSTITUTE FOR BALTIC SEA RESEARCH, SEESTRASSE 15, D-18119 ROSTOCK-WARNEMÜNDE, GERMANY

SCHÜLER, DIRK

DEPT BIOLOGY I, LUDWIG-MAXIMILIANS-UNIVERSITÄT

MÜNCHEN, LMU BIOZENTRUM ZI E 01.028, GROSSHADERNER STR

DEPT OF BIOLOGY, DALHOUSIE UNIVERSITY, HALIFAX,

NOVA SCOTIA, CANADA B3H 4J1

TIELENS, LOUIS

DEPT OF ORGANIC CHEMISTRY, RIJKSUNIVERSITEIT VAN

UTRECHT, CROESESTRAAT 79, UTRECHT, THE NETHERLANDS

WETZEL, MARKUS

INSTITUT FÜR INTEGRIERTE NATURWISSENSCHAFTEN,

ABTEILUNG BIOLOGIE, UNIVERSITY KOBLENZ-LANDAU,

UNIVERSITÄTSSTRASSE 1, 56070 KOBLENZ, GERMANY

We heartily thank all those involved with this book Of course, the book would not be possible without the dedicated efforts of our expert authors We explicitly selected a mixture of World authorities and beginning investigators to be our contributors because we feel that beginning investigators and students will be the leaders in the fi eld in the years to come Also, we selected contributors with differing opinions about the topics at hand In this way, we feel the book reveals the spectrum

of present activities in the fi eld, presents new and emerging insights, and provides

a sound foundation for the reader

However, aside from these expert authors, we must also thank our collaborators who suggested potential author names; their suggestions improved the breadth and scope of this volume In addition, the experienced reviewers, peers, and externals are also heartily thanked Their efforts, sometimes within inconvenient time con-straints, often helped to clarify passages, aiding many authors

Finally, we thank those technicians, laboratory helpers, and administrative professionals who may not be named as authors because science often requires the collaboration of many, sometimes too many, to name formally And, of course,

we thank our families for their patience in our undertaking of this effort Their support and encouragement made the project more enjoyable

Alex Altenbach, Joan Bernhard & Joseph Seckbach (eds.)

GENERAL INTRODUCTION

Fenchel Treude Oren

A.V Altenbach et al (eds.), Anoxia: Evidence for Eukaryote Survival and Paleontological Strategies,

Cellular Origin, Life in Extreme Habitats and Astrobiology 21, 3–16

DOI 10.1007/978-94-007-1896-8_1, © Springer Science+Business Media B.V 2012

Tom Fenchel is an Emeritus Professor of Marine Biology at the University

of Copenhagen He received his Ph.D and his D.Sc from the University of Copenhagen in 1964 and 1969, respectively In the period from 1970 to 1987, he was a Full Professor at the University of Aarhus of zoology and ecology and then became Professor and Director of the Marine Biological Laboratory, University

of Copenhagen 1987–2010 His research has included the ecology and physiology

of microorganisms and evolutionary biology

E-mail: tfenchel@bio.ku.dk