Anoxia: Evidence for Eukaryote Survival and Paleontological Strategies
Abstract
ANOXIA defines the lack of free molecular oxygen in an environment. In the presence of organic matter, the metabolism of anaerobic prokaryotes soon produces compounds such as free radicals, hydrogen sulfide, or methane that are typically toxic to aerobes. The concomitance of suppressed respiration and the presence of toxic substances suggests that these habitats are inhospitable to eukaryotes. Ecological definitions thus sometimes term these environments 'Death Zones'. In this book, however, we present a collection of remarkable adaptations to anoxia, observed in protists, fungi, plants and animals. Presented are case studies that provide evidence for controlled beneficial use of anoxia by, for example, organic modification of free radicals, use of alternative electron donors for anaerobic metabolic pathways, and employment of anaerobic symbionts. Marine, freshwater, and terrestrial organisms and habitats are considered. Ecological, cell biological, and physiological studies are included. In addition to these biologically oriented chapters, the book also presents a paleontological perspective by discussing indirect and direct evidence of eukaryote survival in ancient times. For example, the complex and often interwoven existence of oxic and anoxic milieus in space and time is also highlighted. Finally, we revisit the idea that eukaryotic inhabitation of anoxic habitats was established early in Earth history. This book will certainly increase your concepts regarding abilities of EUKARYOTA.
Chapters (31)
This chapter reviews adaptations to anaerobic life among eukaryotes. While many animals can endure anoxia for extended periods of time, there is no solid evidence that any animal species can complete its life cycle in the complete absence of oxygen. Among the protists (including the fungal chytrids), there are both facultative and obligate anaerobes within many taxonomic groups showing different adaptations to life in the absence of O2. Available evidence suggests that the eukaryotes arose as aerobes, and when extant anaerobic forms are considered, they represent anaerobes that have secondarily adapted to life in anoxic habitats.
This chapter provides an overview of biogeochemical reactions in marine sediments underlying temporal or permanent hypoxic
and anoxic water bodies in modern and past oceans. The aim of this review is to describe the chemical environment that organisms
inhabiting surface sediments encounter during oxygen depletion or deficiency. It also introduces important metabolic processes
that govern or are governed by different redox settings. In Sect. 2, biogeochemical processes in sediments underlying fully
oxygenated water bodies are elucidated. Section 3 explains differences in biogeochemical reactions in hypoxic and anoxic environments
as opposed to oxygenated environments. Modern oxygen minimum zones and permanent anoxic environments are introduced. In Sect.
4 biogeochemical processes during past anoxic events and during the era before the first rise of oxygen are reviewed.
In the last two decades, a number of novel anaerobic processes were discovered in the prokaryotic world that have profoundly
changed our views about the metabolic possibilities in the absence of molecular oxygen. These include the anaerobic oxidation
of ammonium with nitrite as electron acceptor (“the ‘anammox’ process”), anaerobic oxidation of methane coupled with sulfate
reduction using “reverse methanogenesis,” and anaerobic methane oxidation with reduction of nitrite, a process in which a
methanotroph produces its own molecular oxygen needed for the methane monooxygenase reaction by the activity of a nitric oxide
dismutase.
While many multicellular anaerobes possess mitochondria that resemble those of aerobic eukaryotes, microbial eukaryotes that live exclusively in anoxic and low oxygen environments harbor mitochondrion-related organelles (MROs). Currently, these organelles are broadly classified as either hydrogenosomes (anaerobic ATP-producing organelles that produce molecular hydrogen) or mitosomes (organelles that do not generate ATP); however, ongoing studies of diverse microbial lineages are revealing a wider spectrum of functional types. In adaptation to low oxygen conditions, the MROs of anaerobic eukaryotes have acquired unique characteristics, some of which do not appear to derive from the α-proteobacterium that gave rise to the ancestral mitochondrion. These characteristics include alternative pathways for pyruvate metabolism as well as enzymes such as [FeFe]-hydrogenases that collectively function in anaerobic energy metabolism. In addition to these pathways, the mitochondrial protein import, metabolic exchange, and Fe–S cluster biosynthesis machineries are present in all MROs studied to date; these systems support the protein, solute, and energy requirements of both the organelles and the cells that harbor them. MROs represent a unique class of organelles that have successfully adapted by reduction or alteration of existing pathways as well as by acquisition of novel metabolic machineries that allowed their hosts to thrive in diverse environments without oxygen.
Most life forms on the Earth depend on oxygen for continued existence. However, periods of low oxygen (hypoxia) can be tolerated
and are even inherent in normal development and function such as during embryogenesis and strenuous exercise. The process
of adapting to prolonged hypoxia involves activation of a new genetic program which, if not precisely orchestrated, can result
in cell death. It is perhaps not surprising that multiple pathways have evolved for ensuring the up-regulation of essential
genes necessary for hypoxic adaptation. This review will describe mechanisms of cellular adaptation to hypoxia with special
emphasis on vascular endothelial growth factor (VEGF), one of the most ubiquitous and extensively studied hypoxia-inducible
genes. VEGF is known to be up-regulated at the level of transcription and mRNA stabilization due to the action of multiple
factors which can act independently or in concert. A number of mechanisms for targeting specific genes for increased mRNA
translation during hypoxia have been elucidated and will be discussed with respect to VEGF.
Magnetotactic protists of different types have been sporadically observed in a number of aquatic habitats, mainly at the oxic–anoxic transition zone of chemically stratified coastal environments and the anoxic zone. Cells of those examined contained magnetite (Fe3O4) crystals whose size and shape are close to those of magnetotactic bacteria. While some appear to biomineralize their magnetic crystals, others clearly ingest magnetotactic bacteria, with some egesting indigestible remains of these prokaryotes. Magnetotactic protists show a great potential for iron cycling in chemically stratified environments. Many questions remain to be answered regarding these interesting microorganisms.
Oxygen-depleted to anoxic regions of marine environments similar to those found in the Cariaco Trench and the deep Black Sea occur globally and have likely persisted throughout the Earth’s history. Such anaerobic environments have no doubt played an important role in the early formation and evolution of the known biosphere. It is likely that eukaryotes originated prior to the formation of an oxygenated atmosphere (Fenchel and Finlay 1995) and that similar extant anoxic environments may still harbor unknown ancestral lineages. Recent rRNA gene-based surveys of modern anoxic habitats have uncovered diverse communities of anaerobic and aerotolerant organisms that include many novel microscopic eukaryotes (e.g., Dawson and Pace 2002; Stoeck et al. 2003).
The wood-eating termites evolved 140 million years ago in the Early Cretaceous. Symbiotic microbial communities developed
in their hindguts that allowed them to survive on a diet of lignocelluloses, and coevolved into an obligate association that
was vertically transmitted through the colony. A typical gut’s microbial community consists of several types of anaerobic
protists and hundreds of prokaryotes, many of which are specialized to the gut, and include novel chemoautotrophic forms.
Gut-inhabiting protists harbor ecto- and endosymbiotic prokaryotes that have been studied as analogs of early cellular evolution.
Genomic studies have revealed a great deal more molecular genetic diversity in the community than was previously known, and
are producing the first complete genomes of the bacterial endosymbionts. Experimental studies of the community have lagged
because many of the organisms have proven difficult to culture.
A growing number of studies have examined insect survival times during exposure to severe hypoxia and anoxia. Ecologically,
terrestrial insects can be exposed to these conditions during immersion from terrestrial flooding, from encasement in ice
during winter periods, and as a result of specialization to feed in decomposing material, or as internal parasites of vertebrates.
Severe hypoxia has also been tested against a multitude of stored product and museum pests as an alternative to chemical treatment.
Finally, severe hypoxia has been induced experimentally to examine physiological responses of a few model species. Together,
these experiments have revealed a surprising tolerance of insects to severe hypoxia ranging from hours to weeks. In some cases,
ecological studies have revealed apparent adaptation to flooding frequency and duration, while in other cases, the patterns
of survival do not appear to correspond with likely abiotic challenges. This chapter seeks to summarize the body of experimental
work on insects in hypoxia and to serve as a frame of reference for future experiments aimed at elucidating the adaptive significance
of anoxia tolerance by members of the most diverse, ecologically important, and physiologically varied animals on the planet.
Encysted embryos (cysts) of the brine shrimp, Artemia franciscana, appear to bring their overall metabolism to a reversible standstill during prolonged anoxia. Mechanisms involved in this
unusual response are considered, along with the broader significance of cells that survive in the absence of measurable free
energy flow and macromolecular turnover, when fully hydrated and at physiological temperature.
Tardigrades, which are tiny invertebrate animals, have been considered as an appropriate model for astrobiological studies
based on their high survival ability under various types of environmental stresses. So far, researches have shown that tardigrades
have high tolerance to ionizing radiation, wide ranges of temperatures, vacuum, and high pressures in anhydrobiosis, a state
that organisms lack free water in the body, and they resume activity when water is added. In addition, recently, a short-term
flight experiment demonstrated that tardigrades in an anhydrobiotic state survived open space environments at low Earth orbit.
Results from those exposure experiments indicate that tardigrades are well tolerant of extremely low temperatures, vacuum,
and high pressures. On the other hand, ionizing radiation, UV radiation, and high temperatures could be the critical factors
to limit habitable environments for tardigrades. Future astrobiological research on tardigrades, such as long-term exposure
experiments, might provide important insight into the possibilities of existence of animal-like life forms or interplanetary
transfer of multicellular organisms in an anhydrobiotic state.
Tolerance of anoxia is a powerful ecological discriminator for flowering plants. In common with all eukaryotes, all flowering plants require oxygen for cell division. Nevertheless, not all plants need oxygen all the time, and for many species, the ability to survive for a period in an oxygen-deficient environment opens up access to productive habitats in fertile river bottoms, lakes, and marshes. Any plant that survives flooding and temporary impairment of its access to oxygen also has to survive un-flooding. This is a moment of extreme danger as tissues that have been subjected to a prolonged period of anaerobiosis are liable to damage from the generation of active radicals (post-anoxic injury) when they resume aerobic metabolism. This period of post-anoxic injury is directly comparable with post-ischemic injury, which occurs in human patients after heart attacks or organ transplants.
From the poles to the tropics, the ability to survive post-anoxic injury is a characteristic of many plant communities. In the Arctic, plants that survive months of being encased in ice over winter, and thus deprived of access to oxygen, are well endowed with antioxidants against the day when the ice melts and they are once again in free contact with air. Similar situations are found with regard to fluctuating water tables throughout the world. Even drought can impose anoxia when root tissues shrink. Anoxia can also exist in germinating seeds. Drought-resistant seeds frequently have an impermeable seed coat which reduces water loss. However, it also impairs access to oxygen with the result that the developing embryo survives or even begins growth in an anoxic environment. Variation in the many facets of anoxia tolerance is therefore a powerful creator of biodiversity and provides striking examples of the unending capacity of evolution to overcome the potential vicissitudes of fluctuating environments.
Benthic foraminifera, single-celled eukaryotes, constitute a significant part of the living community in low-oxygen or even oxygen-depleted marine environments. Although the diversity is typically low and the dominance high, selected species appears to thrive in such “hostile” environments. In this chapter, the spatial distribution of modern benthic foraminifera, inhabiting the low-oxygen environments from the eutrophic, hypoxic continental shelf settings to the deep ocean oxygen minimum zones (OMZs), is discussed and typical assemblage composition outlined. Furthermore, the in-sediment distribution, or foraminiferal microhabitat, is summarized, and focus is given on species encountered in the deeper hypoxic and anoxic sediment units. Finally, current laboratory experiments and survival strategies including nitrate storage and the physiological role of chloroplasts and bacterial husbandry of foraminifera living in low-oxygen environments are discussed. Recent advances in our understanding of the foraminiferal role in the marine N-cycle and future directions in foraminiferal ecology studies are also addressed.
Laboratory experiments are a valuable way to elucidate physiological and ecological processes of benthic foraminifera under
oxygen-depleted conditions. Experimentally tested survival rates and other experiments show high tolerance of many species
under low oxic to anoxic conditions. Laboratory observations raised different assumptions to explain the physiological adaptations
to this tolerance. Denitrification processes seem to be one important mechanism. Nevertheless, foraminifera try to colonize
sediment horizons with optimal species-specific oxygen concentrations. Experimental settings demonstrated the importance of
oxygen gradients for the orientation in sediments. At the same time, foraminifera change the oxygen concentration in their
microenvironment by respiration. Despite high bioturbation, they do not appear to influence the flux of oxygen into the sediment.
Experimental working in oxygen-depleted environments needs a reliable determination of living foraminifera during the experiment,
e.g., different biochemical techniques. Additionally, electrochemical or optical oxygen sensors that measure the oxygen concentration
are necessary.
Recent benthic foraminifera and their distribution in surface sediments were studied on a transect through the Peruvian oxygen
minimum zone (OMZ) between 10 and 12°S. The OMZ with its steep gradients of oxygen concentrations allows determinations of
the oxygen-dependent changes of species compositions in a relatively small area. Our results from sediments of 13 multicorer
stations from 79 to 823 m water depth demonstrate that calcareous species, especially bolivinids, dominate the assemblages
throughout the OMZ. The depth distribution of several species matches distinct ranges of bottom water oxygen levels. The distribution
pattern inferred a proxy which allows estimating dissolved oxygen concentrations for reconstructing oxygen levels in the geological
past.
The ecology of the benthic foraminiferal community (62–150 and >150 μm) was studied in the continental shelf off Callao (12ºS)
during April 2009. Five sediment stations were sampled along a cross-shelf transect. All the sites were subjected to dysoxic
conditions in the bottom water, but differed in its sedimentary biogeochemical conditions. The inner-shelf, characterized
by high contents of labile organic matter in the sediment surface and sulfidic conditions in the pore water, presented a community
dominated by Bolivina costata, followed by Virgulinella fragilis, a spherical allogromiid morphotype, and Nonionella auris. The outer-shelf, more permanently subjected to the oxygen minimum zone, and characterized by sedimentary suboxic conditions
and lower contents of labile organic matter, was inhabited by a community dominated by Bolivina humilis and Buliminella tenuata. Vertical distributions of V. fragilis, N. auris, and the spherical allogromiid morphotype likely reflect physiological and symbiotic adaptations to anoxia. We conclude that
under this oxygen-deficient setting, the labile organic matter content and the sedimentary redox conditions govern the community
parameters.
“Dead zones” are man-made hypoxic zones (oxygen concentrations of less than 2 mg l−1) that include the seafloor and the water column immediately above it. Such low oxygen concentrations result from the aerobic decay of organic debris from locally elevated primary production that is fueled by anthropogenic nutrient inputs to the coastal ocean (e.g., fertilizer runoff). Other benthic environments with persistent hypoxia unrelated to human activities have been known for decades. Silled basins and cold seeps are examples of natural hypoxic regions. Using microscopy, we have documented disparate, diverse, symbioses-dominated assemblages of protists as well as nematodes from all three of these hypoxic environments. The “dead zone” off the Mississippi River is dominated by flagellates and ciliates. In contrast, Monterey Bay cold seeps, while hosting biomass roughly equivalent to that from the Mississippi “dead zone,” had assemblages dominated by nematodes. The assemblage from Santa Barbara Basin was approximately an order of magnitude higher in biomass and was dominated by foraminifera. In all three hypoxic environments, symbioses were a prominent component of the assemblage and are likely the factor that allows these assemblages to thrive.
Anoxia is a key issue in the past and present marine ecosystems. This is because no other form of disturbance so severely
affects marine communities over such extensive areas. Anoxia is also the only manifestation of human-induced disturbance that
was also an important factor in ancient systems. While microorganisms may rule the Earth, it is fundamentally the macrofauna
that defines marine ecosystems and provides the ecosystem services on which we rely. Recurrent or intermittent hypoxia and
anoxia represent the least consistent and therefore the most extreme habitat conditions for benthic communities. The unpredictable
and rapid onset of anoxia-related mortalities has hampered our ability to document and understand the reactions of benthic
organisms. One approach is to experimentally recreate, on a small-scale, hypoxia and anoxia in situ. We have designed and
deployed an experimental anoxia generating unit (EAGU), equipped with time-lapse camera and sensor arrays, to analyze the
behaviors and mortality sequences of benthic macrofauna in the Northern Adriatic (Mediterranean Sea), a model for eutrophication-related
low dissolved oxygen events. This yields information that helps evaluate the condition and status of benthic communities,
including in ancient marine ecosystems.
The Black Sea contains the World’s largest body of anoxic water. Based on new and published data, we describe trends among
selected protozoan and metazoan meiofaunal taxa at water depths of 120–240 m in the northwestern part of the Black Sea near
the submarine Dnieper Canyon. This transect spans the transition between increasingly hypoxic but non-sulfidic bottom water
and the deeper anoxic/sulfidic zone, the boundary between these two domains being located at approximately 150–180 m depth.
This transition zone supports a rich rose-Bengal-stained fauna. Among the protozoans, gromiids are common only at 120 and
130 m. All other groups exhibit more or less distinct abundance maxima near the base of the hypoxic zone. Foraminifera peak
sharply at ∼160 m while ciliates are most abundant at 120, 160–190, and 240 m, where they are possibly associated with concentrations
of bacterial cells. The three most abundant metazoan taxa also exhibit maxima in the hypoxic zone, the nematodes and polychaetes
at 160 m, and the harpacticoid copepods at 150 m. Most of the polychaetes belong to two species, Protodrilus sp. and Vigtorniella zaikai, the larvae of which are widely distributed in severely hypoxic water just above the anoxic/sulfidic zone of the Black Sea.
Both protozoans and metazoans are usually concentrated in the 0–1 cm layer of the sediment, except at the shallowest (120–130
m) site where deeper layers may yield a substantial proportion of the assemblage. The concentration of nematodes in the 3–5
cm layer at 120 m is particularly notable. Our data suggest that some benthic species can tolerate anoxic/sulfidic conditions
in the Black Sea. An important caveat is that anoxia or severe hypoxia may lead to the corpses of nonindigenous organisms
being preserved in our samples. However, we argue that the morphological integrity of specimens, the high population densities
(associated with high bacterial concentrations in the case of ciliates), the presence of taxa often found in hypoxic settings,
and the presence of all life stages (including gravid females) among nematodes and harpacticoids, suggests that at least some
of the organisms are indigenous. Further comparative studies of shallow- and deep-water meiobenthic communities in the Black
Sea are necessary in order to establish which species are characteristic and indicative of hypoxic/anoxic conditions.
The importance of anaerobic free-living phagotrophic protists has gained renewed attention following the discovery of an unexpectedly high diversity in anoxic aquatic habitats. Here I attempt to illustrate the physiology and trophic role of phagotrophic protists in anoxic compartments of chemically stratified lakes. The long-standing notion of the low productivity of anaerobic food webs is partly disputed and the possibility of aerobic metazoans that are able to withstand anoxia acting as a trophic link between anaerobic primary production and the aerobic food web of metazoans is briefly covered.
The origin of eukaryotes in an anoxic versus an oxygenated environment is controversially discussed. To date, no conclusive
data are available to decide this debate for the one or for the other camp. Yet, a substantial data set, coming from the anaerobic
biochemistry of extant eukaryotes, the modeling of Proterozoic ocean chemistry, and earth’s history (specifically when considered
in concerto), provides reasonable evidence for the hypothesis of an early eukaryote evolution in an anoxic world, which is
summarized in the first part of this chapter. Contemporary anoxic and sulfidic environments are the stage on which to find
the key players that can help to strengthen this view. We, in the second part of this chapter, present an ideal natural model
system – the supersulfidic, anoxic Framvaren Fjord in south Norway – to study the evolution and diversity of unicellular eukaryotes
– the protists – and summarize the knowledge that has been accumulated from the Framvaren Fjord in this field of research,
evidencing the importance of such systems in evolution and biodiversity research.
Although a relatively high diversity of eukaryotic organisms exists in anoxic habitats, these extreme environments are mainly characterized by their prokaryotic communities. The meromictic alpine Lake Alat in Bavaria, Germany exhibits a stable chemocline throughout the year. In contrast to many other freshwater habitats, the purple sulfur bacteria bloom is a thick, well-defined layer. The different bacterial assemblages involved in the sulfur cycle create a stable and permanent environment. Chemical and thermal stratification make this lake a very unique lentic habitat. The thermo- and the chemocline were described by measurements of physical parameters, such as temperature, oxygen, and conductivity, as well as the chemobiological measurements of particulate organic carbon and nitrogen concentrations. With the analyses of environmental DNA samples, we studied the bacterial diversity within this thermocline. Universal bacterial 16S rDNA as well as specific Chromatiaceae 16S rDNA PCR were cloned. Analyses showed that almost all randomly chosen clones were among γ-proteobacteria more specifically; sequences are most similar to the family Chromatiaceae, but few δ-proteobacteria occur.
The discovery of the chemolithotrophy-based groundwater ecosystem at Ayyalon in Israel served to propose the new speleological
paradigm of the Ophel biome. After briefly dealing with the biota of Ayyalon and their biology, some aspects of possible physiological
adaptation of the subterranean crustacean fauna to subterranean hypoxia and anoxia are presented. The extremophily of ophelic
crustaceans and its paleo-historical significance is suggested.
Marine sediments cover more than two-thirds of the Earth’s surface and have been estimated to contain as much as one-third
of Earth’s prokaryotic biomass (Whitman et al. 1998). Despite this, relatively little is known about this deep biosphere,
and essentially nothing is known about the presence of microbial eukaryotes (protists) in sediments deeper than a few centimeters.
Through consumption of dissolved organic matter and by selective grazing in subsurface horizons where bacterial and/or archaeal
numbers are high, protists may significantly impact carbon cycling in the marine subsurface. An understanding of the biogeochemical
activities, composition, and temporal and spatial dynamics of marine subsurface communities is essential for accurate modeling
of nutrient cycling in this vast subsurface biosphere.
Knowledge about the biogeochemistry of nitrogen cycling in modern aquatic ecosystems and the associated fractionations of
nitrogen isotopes (δ15N) has increased significantly during the past two decades. These insights also improved our ability to interpret δ15N records recovered from ancient sediments. Specific environmental setups such as coastal upwelling areas, open pelagic realms,
or stagnant basins are characterized by distinct biogenic processes and the formation of a typifying sedimentary record. We
find growing evidence to recover these distinct biogenic processes in detail from δ15N patterns observed in earth history. Sediments with elevated nitrogen contents (>0.2%) and low diagenetic offprint are most
suitable for such investigations. The analysis of δ15N in extracted biomarkers such as chlorines and porphyrines, or from nitrogen bearing hard parts of certain fossils offer
valuable tools to assess the sample quality and a possible imprint derived from diagenesis.
Our study aims to record carbon and nitrogen isotopic fractionations in Foraminifera recovered from the sulfidic and long term anoxic environment of the Namibian diatomaceous mud belt. Two species which can be considered facultative anaerobes were investigated, Virgulinella fragilis
Grindell and Collen and Nonionella stella
Cushman and Moyer. The former species shelters presumably chemotrophic bacteria as endosymbionts and utilizes electron acceptors other than dissolved oxygen (Bernhard 2003; Tsuchia et al. 2006), and the latter species accumulates large quantities of intracellular nitrate for denitrification (Risgaard-Petersen et al. 2006; Høgslund 2008; Høgslund et al. 2008) and sequesters chloroplasts (Bernhard and Bowser 1999; Grzymski et al. 2002).KeywordsDissolve Inorganic CarbonAnaerobic Ammonia OxidationBenthic ForaminiferaRose BengalCarbon Isotopic FractionationThese keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This chapter will give a brief review about the present understanding of pores in tests of benthic foraminifera. The interpretation of the pore function changed through time, and a couple of theories were proposed. The research about the functionality of pores recently became of new interest because it seems likely that they are involved in the respiration pathways of some benthic foraminifera. The fact that several benthic species are able to survive anoxia points out the importance for a better understanding of these respiration pathways and which adaptions differentiate these species from species which cannot survive in oxygen-depleted habitats. Nitrate respiration seems to be widespread among foraminifera from oxygen-depleted habitats, and thus knowledge if and in how far the pores are involved in the process of denitrification would help to understand the process of denitrification in eukaryotic foraminiferal cells.
Anoxic conditions prevailed on the Late Cretaceous seafloor beneath a long-term upwelling system situated across the southern Tethys. In Israel, the acme of this system was during the Campanian, when a suite of characteristic lithofacies (organic-rich carbonate, phosphorite, porcelanite, and chert) was broadly distributed over at least a 250 km wide zone encompassing the paleotopography of the Syrian Arc fold belt and beyond. Stressed faunal associations developed all across this belt. While more ventilated horizons supported molluscan assemblages, laminated sediments with oxygenation levels below 0.1 ml O2/l were macroscopically sterile but were found to support rich foraminiferal microfaunas. These faunas, apparently adapted to near anoxia, are dominated by two highly specialized buliminid species, Neobulimina canadensis and Praebulimina prolixa, in five assemblages that define different levels of oxygen stress. The foraminifera presumably lived below the sediment surface in the pore-water microenvironment, where habitat partitioning depended on food and oxygen resources rather than the nature of the sediment particles. They therefore do not correlate to the sediment type or lithofacies from which they were recovered.
Agglutinated foraminifera are benthic organisms that in modern sediments have been described from marginal marine to bathyal environments. A number of modern taxa have adapted well to oxygen-deficient environments, but even those require at least some oxygen in order to persist at the seafloor. Agglutinated foraminifera in sediments from the central deep of the Santa Barbara Basin are typically multi-chambered and have walls that incorporate a variety of silicate minerals. Some taxa are quite selective with regard to mineral type and size, whereas others seem to incorporate a wide range of minerals and grain sizes. With deeper burial, these foraminifera tests collapse and give rise to mineral streaks that are distinct through comparatively narrow sorting and grain-type variability. Collapsed agglutinated foraminifera with mono-mineralic as well as mixed mineral walls have been observed in black shale samples of Devonian to Mississippian age, suggesting benthic assemblages comparable to those seen in modern and sub-recent Santa Barbara Basin muds. The latter thrive in a largely suboxic setting and suggest by analogy that extended bottom water anoxia, though frequently postulated, was not a requirement for the formation of Paleozoic black shales. Improved criteria for the recognition of benthic agglutinated foraminifera in the rock record should help to bring new perspectives to the ongoing debate about the origin of ancient black shale successions and accelerate the removal of simplistic models from the discussion.
The genetically controlled formation of shells (“tests”) in the protistan first-rank Foraminifera [Rhizaria] offers a considerable
advantage in evolutionary and phylogenetic studies on their development and diversification. Fossilized tests reveal the evolutionary
patterns for some thousand genera, from the Cambrian to the Holocene.
The history of the Earth, its lithosphere, hydrosphere, atmosphere, and biosphere is closely interlinked in many disciplines (geology, paleoclimatology, paleoceanography, and geobiology or paleobiology). This relationship is particularly complicated for the Precambrian constituting c. 90% of this history. When stepping backward in time, the history is increasingly obliterated by alteration processes connected to plate tectonics, metamorphism, diagenesis, biodegradation and taphonomy, and simply by increasing coverage by younger rocks. The biggest problems in deciphering this history are imposed by the often diametrically controversial interpretation of lithological, biological, and geochemical signatures preserved from these times, but especially from the Precambrian far past, the Archean (4.6–2.5 billion years ago). The most intriguing problems in our understanding of the earliest c. 60% of the Earth’s history are: the geochemistry of the primordial oceans and atmosphere, their pH and oxidation state, and mineralization processes, e.g., the origin of banded iron formations; periods of global glaciations (Snowball Earth scenarios); and the appearance and early evolution of life, including photosynthesis, cyanobacteria, prokaryotes, and eukaryotes. A comprehensive overview of these problems and the discussed solutions can be gained from the series of state-of-the-art articles treating the entire Precambrian period, in Eriksson et al. (2004). Moreover, an all-embracing view on the close relationships of mineralogy and biology and the general evolution of the Earth and the lithosphere and biosphere can be detracted from Hazen et al. (2008). The present contribution is partly based on these discussions, perhaps not familiar to a wide audience of microbiologists.
... The pore density in the shells of Bolivina spissa is significantly correlated to the [NO 3 − ] in their habitats because the pores facilitate the uptake of electron acceptors for respiration 17 . A comprehensive review about the functionality of pores in benthic foraminifera can be found in ref. 18 . The functionality of pores in Foraminifera ranges from gas exchange for the uptake of electron acceptors and the release of metabolic waste products like CO 2 19 to the uptake of dissolved organic material 20 . ...
... We reconstructed bottom water NO 3 − concentrations ([NO 3 − ] BW ) using sediment core M77/2 52-2 (5°29′S; 81°27′W; 1250 m) from the Peruvian continental margin over the last deglaciation. Past [NO 3 − ] BW was reconstructed using the pore density of the benthic foraminiferal species B. spissa (Fig. 1a 18 . The pore densities of 819 specimens were analyzed for this record to provide a statistically robust dataset in a sufficient temporal resolution (Fig. 1a) − ] BW ) occurred during the LGM. ...
Anthropogenic impacts are perturbing the global nitrogen cycle via warming effects and pollutant sources such as chemical fertilizers and burning of fossil fuels. Understanding controls on past nitrogen inventories might improve predictions for future global biogeochemical cycling. Here we show the quantitative reconstruction of deglacial bottom water nitrate concentrations from intermediate depths of the Peruvian upwelling region, using foraminiferal pore density. Deglacial nitrate concentrations correlate strongly with downcore δ13C, consistent with modern water column observations in the intermediate Pacific, facilitating the use of δ13C records as a paleo-nitrate-proxy at intermediate depths and suggesting that the carbon and nitrogen cycles were closely coupled throughout the last deglaciation in the Peruvian upwelling region. Combining the pore density and intermediate Pacific δ13C records shows an elevated nitrate inventory of >10% during the Last Glacial Maximum relative to the Holocene, consistent with a δ13C-based and δ15N-based 3D ocean biogeochemical model and previous box modeling studies.
... There is currently a renewed interest in the role of microbial eukaryotes in the ecology of extreme environments, including anoxic and hypoxic habitats (Fenchel 2012; within Intramacronucleata has been clarified by analysis of more extensive molecular data with the recognition of the "SAL" (Spirotrichea + Armophorea + Litostomatea) superclade Gentekaki et al. 2014). Jankowski (2007) divided Armophorea into four orders: mostly free-living Armophorida (caenomorphids) and Metopida (metopids), endobiotic Clevelandellida, and Odontostomatida. ...
... Although cytoplasmic endosymbionts were inconspicuous in vivo in those strains of M. es and B. contorta studied in detail, and impregnated inconsistently with protargol (Fig. 2C), we have observed endosymbionts in TEM preparations (not shown) and both species are known to harbor methanogenic archaea (Finlay and Fenchel 1992;Hackstein 2010). The free-living metopid ciliates constitute a fascinating intersection between these highly adapted microbial eukaryotes, free-living prokaryotes, and prokaryote endo-and ectosymbionts (Fenchel 2012;Saccà 2012;Tsaousis et al. 2012). They provide potential systems for the elucidation of biogeochemical cycling, the evolution of eukaryote-prokaryote symbioses, and the varied adaptations required for eukaryotic existence in anoxic environments (Edgcomb et al. 2007;Fenchel and Ramsing 1992;Germond and Nakajima 2016;Gil et al. 2016;Hackstein 2010;Hu 2014;Yarlett and Hackstein 2005). ...
... A few live brine shrimp were observed from 16 h to 48 h for 0 rpm. For 0 rpm, cysts accumulated at the bottom of the flask and were subjected to anaerobic conditions, which interrupted cyst development (Sorgeloos 1980, Clegg 2012. The CHNs of 400 rpm were also small and gradually decreased from 16 h to 28 h. ...
Hydration plays a particularly important role in health maintenance and general well-being. A wide assortment of drinking waters are currently available on the market. However, their ability to hydrate may vary. For studying hydration, a useful organism may be the cysts of brine shrimp. Those cysts may remain dehydrated and functionless for years, but regain function once hydrated. In this study, we first determined the optimal factors for assessing hydration in the brine-shrimp model, including aeration method and flow rate, salinity, and temperature. Various kinds of water, including tap water, bottled water, and water containing health-promoting agents, were tested by using this new method to evaluate their ability to hydrate. Tap water showed weak hydration, while some bottled waters (e.g., Kirkland Signature Purified Water) hydrated more effectively. Mineral water, such as Fiji water, was found to be a desirable option to maintain adequate and lasting hydration.
Graphic abstract
... anoxic-no dissolved oxygen, dysoxic-0.1-1 ml/l; Altenbach et al. 2011;Sen Gupta 1999) bottom-water environments. The combination of foraminiferal records and geochemical proxies allowed us to recognize faunal shifts and their environmental settings and to take a further step in inferring specific biological evolutionary adaptations that enabled benthic foraminifera to successfully colonize anoxic-dysoxic environments, in a similar manner as their modern successors. ...
Waterfalls are conspicuous geomorphological features with heterogeneous structure, complex dynamics and multiphase flows. Swifts, dippers and starlings are well-known to nest behind waterfalls, and have been reported to fly through them. For smaller fliers, by contrast, waterfalls seem to represent impenetrable barriers, but associated physical constraints and the kinematic responses of volant animals during transit are unknown. Here, we describe the flight behaviour of hummingbirds (the sister group to the swifts) and of various insect taxa as they fly through an artificial sheet waterfall. We additionally launched plastic balls at different speeds at the waterfall so as to assess the inertial dependence of sheet penetration. Hummingbirds were able to penetrate the waterfall with reductions in both their translational speed, and stroke amplitude. The body tilted more vertically and exhibited greater rotations in roll, pitch and yaw, along with increases in tail spread and pitch. The much smaller plastic balls and some flies moving at speeds greater than 2.3 m s ⁻¹ and 1.6 m s ⁻¹ , respectively, also overcame effects of surface tension and water momentum and passed through the waterfall; objects with lower momentum, by contrast, entered the sheet but then fell along with the moving water. Waterfalls can thus represent impenetrable physical barriers for small and slow animal fliers, and may also serve to exclude both predators and parasites from nests of some avian taxa.
... anoxic-no dissolved oxygen, dysoxic-0.1-1 ml/l; Altenbach et al. 2011;Sen Gupta 1999) bottom-water environments. The combination of foraminiferal records and geochemical proxies allowed us to recognize faunal shifts and their environmental settings and to take a further step in inferring specific biological evolutionary adaptations that enabled benthic foraminifera to successfully colonize anoxic-dysoxic environments, in a similar manner as their modern successors. ...
It is widely acknowledged that life has adapted to its environment, but the precise mechanism remains unknown since Natural Selection, Descent with Modification and Survival of the Fittest are metaphors that cannot be scientifically tested. In this unique text invertebrate and vertebrate biologists illuminate the effects of physiologic stress on epigenetic responses in the process of evolutionary adaptation from unicellular organisms to invertebrates and vertebrates, respectively. This book offers a novel perspective on the mechanisms underlying evolution.
Capacities for morphologic alterations and epigenetic adaptations subject to environmental stresses are demonstrated in both unicellular and multicellular organisms. Furthermore, the underlying cellular-molecular mechanisms that mediate stress for adaptation will be elucidated wherever possible. These include examples of ‘reverse evolution’ by Professor Guex for Ammonites and for mammals by Professor Torday and Dr. Miller. This provides empirical evidence that the conventional way of thinking about evolution as unidirectional is incorrect, leaving open the possibility that it is determined by cell-cell interactions, not sexual selection and reproductive strategy. Rather, the process of evolution can be productively traced through the conservation of an identifiable set of First Principles of Physiology that began with the unicellular form and have been consistently maintained, as reflected by the return to the unicellular state over the course of the life cycle.
... anoxic-no dissolved oxygen, dysoxic-0.1-1 ml/l; Altenbach et al. 2011;Sen Gupta 1999) bottom-water environments. The combination of foraminiferal records and geochemical proxies allowed us to recognize faunal shifts and their environmental settings and to take a further step in inferring specific biological evolutionary adaptations that enabled benthic foraminifera to successfully colonize anoxic-dysoxic environments, in a similar manner as their modern successors. ...
The goal of this chapter is to discuss old problems and recent polemics related to the famous Cope’s, Dollo’s and Haeckel’s rules. The first concerns phyletic size increase: that sort of trend is observed in a multitude of phyla and shows several exceptions during periods of environmental stress. The second rule is discussed with some details because evolutionary reversions of trends are also frequent during stress episodes. The third trend, terminal addition, is very common and one can observe numerous cases where characters that are added late in phylogeny are also the first to be deleted during external stress phases. The addition of new elements at the end of ontogeny is frequently concomitant with size increases (Cope’s trend).
... anoxic-no dissolved oxygen, dysoxic-0.1-1 ml/l; Altenbach et al. 2011;Sen Gupta 1999) bottom-water environments. The combination of foraminiferal records and geochemical proxies allowed us to recognize faunal shifts and their environmental settings and to take a further step in inferring specific biological evolutionary adaptations that enabled benthic foraminifera to successfully colonize anoxic-dysoxic environments, in a similar manner as their modern successors. ...
Planktic foraminifera, unicellular microzooplankton with a calcitic shell, have produced an exceptional fossil record, revealing an invaluable archive of biodiversity, morphological and evolutionary changes. The evolutionary lineage starting from Trilobatus Spezzaferri 2015 (= “Globigerinoides”) culminating in Orbulina universa d’Orbigny 1839 is a fascinating example of peramorphic spherisation lineage (increasing involution, coupled with increasing shell curvature). This chapter focuses on the extreme morphological variability observed in the Orbulina group in some horizons from Chélif Basin in Algeria, just preceding the well-known Messinian (Late Miocene) salinity crisis in the Mediterranean basin. Surprisingly, in such horizons, spherical Orbulina universa lineage end-member specimens coexist with ancestor-like morphotypes, such as Orbulina suturalis Brönnimann 1951 and the supposed extinct Praeorbulina Olsson 1964, as well as with malformed specimens. Many authors considered in fact that Praeorbulina last occurred within the Langhian stage in the Middle Miocene. A similar recovery of individuals which show an intergradation between a typical Orbulina morphology and morphologies close to the ancestors Orbulina suturalis and Praeorbulina was also reported in Last Glacial Maximum sediments from the northern Arabian Sea. In this Late Pleistocene case, AMS 14C data showed clearly unreworked character of this “Praeorbulina-like” populations. We discuss the possible link between this extreme morphological plasticity of Orbulina group in specific time horizons and possible stress conditions of the water column.
... anoxic-no dissolved oxygen, dysoxic-0.1-1 ml/l; Altenbach et al. 2011;Sen Gupta 1999) bottom-water environments. The combination of foraminiferal records and geochemical proxies allowed us to recognize faunal shifts and their environmental settings and to take a further step in inferring specific biological evolutionary adaptations that enabled benthic foraminifera to successfully colonize anoxic-dysoxic environments, in a similar manner as their modern successors. ...
Following a multi-proxy analysis of the Upper Cretaceous high-productivity sequence from proximal and distal basins in Israel, Meilijson et al. (Paleobiology 42:77–97, 2016) provided evidence indicating that different benthic foraminifera species could survive and sustain large populations under long-term anoxic to dysoxic bottom water conditions. They proposed that massive blooms of triserial (buliminid) benthic foraminifera with distinct apertural and test morphologies during the Campanian managed to survive anoxic conditions by their capability to sequester diatom chloroplasts (kleptoplastidy) and associate with bacteria, in a similar manner as their modern analogues. This advantageous capability as well as other adaptations such as using nitrate instead of oxygen for their respiratory pathways, or changes in food type arriving to the seafloor, were all affected by the substantial shift in the depositional environment following the Campanian/Maastrichtian boundary. However, several of the hypothesis and assumptions presented in this chapter called for a continued study of the Upper Cretaceous deposits in the Levant, to better constrain the oceanographic and bottom water process in which these organisms lived.
... anoxic-no dissolved oxygen, dysoxic-0.1-1 ml/l; Altenbach et al. 2011;Sen Gupta 1999) bottom-water environments. The combination of foraminiferal records and geochemical proxies allowed us to recognize faunal shifts and their environmental settings and to take a further step in inferring specific biological evolutionary adaptations that enabled benthic foraminifera to successfully colonize anoxic-dysoxic environments, in a similar manner as their modern successors. ...
Herein we emphasise how environment, palaeoecology and palaeobiogeography play key roles in the evolution of organisms. Nineteenth-century ammonoid biochronology led to the definition of the Mesozoic stages. Their beginning and end are bound by the biggest mass extinctions of Earth history. This study deals with the initial Triassic stages that needed a remarkably short biotic recovery time. The Lower Triassic stages, all named after nineteenth-century researchers of the Himalayas, are the Griesbachian, Dienerian, Smithian and Spathian.
... anoxic-no dissolved oxygen, dysoxic-0.1-1 ml/l; Altenbach et al. 2011;Sen Gupta 1999) bottom-water environments. The combination of foraminiferal records and geochemical proxies allowed us to recognize faunal shifts and their environmental settings and to take a further step in inferring specific biological evolutionary adaptations that enabled benthic foraminifera to successfully colonize anoxic-dysoxic environments, in a similar manner as their modern successors. ...
In “On the Origin of Species,” Darwin describes the terrain of Patagonia at great length during his voyage on the HMS Beagle. From that experience, he inferred the importance of the environment in understanding the adaptive evolution of flora and fauna. To this day, and despite the passage of time, observations of the interrelationship between the complexity of environmental stresses and their relevance to evolution remain inferential rather than proven through rigorous scientific measurement. In the Galapagos, the Grants have attempted a distinct longitudinal study of the interrelationship between the environment and adaptive phenotype. However, their scrutiny of finch beaks and size is confounded with substantial observational bias, included no rigorous species definitions, and answered no substantive evolutionary questions since no novelty was observed (Grant, P. R., Grant, B. R. How and Why Species Multiply: The Radiation of Darwin’s Finches. Princeton University Press, 2011).
... When encountering water with low oxygen (hypoxic) or no oxygen (anoxic), some ophiuroids, such as Ophiothrix Müller & Troschel, 1840, widen the bursal slits, perhaps allowing movement of a greater volume of water by ciliary current (Austin, 1966). Some species exhibit a behavior called "arm-tipping," where the ophiuroid stands up on its arm tips, raising the disc up higher in the water column, presumably in an effort to reach more oxygenated waters (Altenbach et al., 2012;Riedel et al., 2014). Others often attempt to quickly vacate the immediate area by climbing nearby structures or by moving away in a lateral direction. ...
The basket star Gorgonocephalus eucnemis is an aerobic organism highly dependent on dissolved oxygen in surrounding waters. Previous observations on the anatomy of Gorgonocephalus state that five pairs of ossicles (the radial shields and genital plates) regulate the position of the roof of the body disc and are responsible for flushing seawater into and out of the bursae, though this seems never to have been empirically tested. In the current study, rates of bursal ventilation were investigated in response to an increase in the availability of food and, separately, exposure to hypoxic levels of dissolved oxygen. When fed with suspended krill particles, basket stars increased rates of bursal ventilation, ranging from 13% to 155%, resulting in a similar increase in volume of water moved in and out of bursae. This rate remained elevated for an average of 25 minutes after active feeding ended. Bursal ventilation rates also increased significantly (~60% average increase) when basket stars were exposed to hypoxic conditions (dissolved oxygen ≤ 3.5 mg O2 L-1 = 2.45 mL O2 L-1). Some specimens exhibited a loss of coordination in hypoxic conditions. All specimens recovered and resumed a normal rate of bursal ventilation when returned to normoxic conditions. Measurements show that dissolved oxygen levels decreased from outside to inside bursae and suggest that dissolved oxygen is absorbed in bursae during bursal ventilations. Increasing rates of bursal ventilation may help meet the increased oxygen demands when feeding and may help animals endure some exposures to hypoxia.
... Here we present new evidence from the Late Cretaceous Levantine high productivity sequence (upper Menuha, Mishash, and lower Ghareb formations), which show that different benthic foraminifera species with diverse morphologies were able to tolerate and successfully colonize anoxic-dysoxic (i.e., anoxic = no dissolved oxygen, dysoxic = 0.1-1 ml/l; Bernhard and Sen Gupta 1999;Altenbach et al. 2012) bottom water environments. This unique depositional environment was investigated using a combination of foraminiferal records and diverse geochemical proxies analyzed in the same samples. ...
... In the literature, the terminology and threshold values used to describe oxygen depletion are highly variable (e.g. oxic, dysoxic, hypoxic, suboxic, microxic, postoxic; see Jorissen et al., 2007;Altenbach et al., 2012). In this study we defined hypoxia as a concentration of oxygen < 63 µmol L −1 (1.4 mL L −1 or 2 mg L −1 ) whereas anoxia is defined as no detectable oxygen (following Rabalais et al., 2010). ...
Over the last decades, hypoxia in marine coastal environments has become more and more widespread, prolonged and intense. Hypoxic events have large consequences for the functioning of benthic ecosystems. In severe cases, they may lead to complete anoxia and the presence of toxic sulfides in the sediment and bottom-water, thereby strongly affecting biological compartments of benthic marine ecosystems. Within these ecosystems, benthic foraminifera show a high diversity of ecological responses, with a wide range of adaptive life strategies. Some species are particularly resistant to hypoxia–anoxia, and consequently it is interesting to study the whole foraminiferal community as well as species-specific responses to such events. Here we investigated the temporal dynamics of living benthic foraminiferal communities (recognised by CellTracker™ Green) at two sites in the saltwater Lake Grevelingen in the Netherlands. These sites are subject to seasonal anoxia with different durations and are characterised by the presence of free sulfide (H2S) in the uppermost part of the sediment. Our results indicate that foraminiferal communities are impacted by the presence of H2S in their habitat, with a stronger response in the case of longer exposure times. At the deepest site (34 m), in summer 2012, 1 to 2 months of anoxia and free H2S in the surface sediment resulted in an almost complete disappearance of the foraminiferal community. Conversely, at the shallower site (23 m), where the duration of anoxia and free H2S was shorter (1 month or less), a dense foraminiferal community was found throughout the year except for a short period after the stressful event. Interestingly, at both sites, the foraminiferal community showed a delayed response to the onset of anoxia and free H2S, suggesting that the combination of anoxia and free H2S does not lead to increased mortality, but rather to strongly decreased reproduction rates. At the deepest site, where highly stressful conditions prevailed for 1 to 2 months, the recovery time of the community takes about half a year. In Lake Grevelingen, Elphidium selseyense and Elphidium magellanicum are much less affected by anoxia and free H2S than Ammonia sp. T6. We hypothesise that this is not due to a higher tolerance for H2S, but rather related to the seasonal availability of food sources, which could have been less suitable for Ammonia sp. T6 than for the elphidiids.
... However, the presence of RNA transcripts (i.e., mRNA) strongly indicates that some nematode species were alive and metabolically active in this DZS. Nematodes are known to tolerate hypoxia 15,31,32 , and have been observed, e.g., in the Gulf of Mexico and Black Sea dead zones 33,34,35 . Benthic nematodes can temporarily cope with anoxia by migrating upward to the overlying oxic water until normoxic conditions return to the sediment 32 . ...
Ocean deoxygenation driven by global warming and eutrophication is a primary concern for marine life. Resistant animals may be present in dead zone sediments, however there is lack of information on their diversity and metabolism. Here we combined geochemistry, microscopy, and RNA-seq for estimating taxonomy and functionality of micrometazoans along an oxygen gradient in the largest dead zone in the world. Nematodes are metabolically active at oxygen concentrations below 1.8 µmol L−1, and their diversity and community structure are different between low oxygen areas. This is likely due to toxic hydrogen sulfide and its potential to be oxidized by oxygen or nitrate. Zooplankton resting stages dominate the metazoan community, and these populations possibly use cytochrome c oxidase as an oxygen sensor to exit dormancy. Our study sheds light on mechanisms of animal adaptation to extreme environments. These biological resources can be essential for recolonization of dead zones when oxygen conditions improve.
These authors contributed equally: Elias Broman, Stefano Bonaglia.
... Due to the thermal stratification 105 and high oxygen consumption in the benthic compartment, development of bottom water hypoxia/anoxia occurs in the deepest part of the basin in summer to early autumn (Bannink et al., 1984;Hagens et al., 2015). In the literature, the terminology and threshold values used to describe oxygen depletion are highly variable (e.g., oxic, dysoxic, hypoxic, suboxic, microxic, postoxic; see Jorissen et al., 2007;Altenbach et al., 2012). In this study we defined hypoxia by a concentration of oxygen <63 µmol L -1 (1.4 mL L -1 or 2 mg L -1 ) whereas anoxia is defined as no detected oxygen (following Rabalais et al., 2010). ...
... Due to the thermal stratification 105 and high oxygen consumption in the benthic compartment, development of bottom water hypoxia/anoxia occurs in the deepest part of the basin in summer to early autumn (Bannink et al., 1984;Hagens et al., 2015). In the literature, the terminology and threshold values used to describe oxygen depletion are highly variable (e.g., oxic, dysoxic, hypoxic, suboxic, microxic, postoxic; see Jorissen et al., 2007;Altenbach et al., 2012). In this study we defined hypoxia by a concentration of oxygen <63 µmol L -1 (1.4 mL L -1 or 2 mg L -1 ) whereas anoxia is defined as no detected oxygen (following Rabalais et al., 2010). ...
Over the last decades, hypoxia in marine coastal environments have become more and more widespread, prolonged and intense. These hypoxic events have large consequences for the functioning of benthic ecosystems. They profoundly modify early diagenetic processes involved in organic matter recycling, and in severe cases, they may lead to complete anoxia and presence of toxic sulphides in the sediment and bottom water, thereby severely affecting biological compartments of benthic marine ecosystems. Within these ecosystems, benthic foraminifera show a high diversity of ecological responses, with a wide range of adaptive life strategies. Some species are particularly resistant to hypoxia/anoxia and consequently, it is interesting to study the whole foraminiferal community as well as species specific responses to such events. Here we investigated the temporal dynamics of living benthic foraminiferal communities (recognised by CellTracker™ Green) at two sites in the saltwater Lake Grevelingen in the Netherlands. These sites are subject to seasonal anoxia with different durations and are characterised by the presence of free sulphide (H2S) in the uppermost part of the sediment. Our results indicate that foraminiferal communities are impacted by the presence of H2S in their habitat, with a stronger response in case of longer exposure times. At the deepest site (34 m), one to two months of anoxia and free H2S in the surface sediment resulted in an almost complete disappearance of the foraminiferal community. Conversely, at the shallower site (23 m), where the duration of anoxia and free H2S was shorter (one month or less), a dense foraminiferal community was found throughout the year. Interestingly, at both sites, the foraminiferal community showed a delayed response to the onset of anoxia and free H2S, suggesting that the combination of anoxia and free H2S does not lead to increased mortality, but rather to strongly decreased reproduction rates. At the deepest site, where highly stressful conditions prevailed for one to two months, the recovery time of the community takes about half a year. In Lake Grevelingen, Elphidium selseyense and Elphidium magellanicum are much less affected by anoxia and free H2S than Ammonia sp. T6. We hypothesise that this is not due to a higher tolerance of H2S, but rather related to the seasonal availability of food sources, which could have been less suitable for Ammonia sp. T6 than for the elphidiids.
... His publications were sometimes controversial and, as he wrote himself, reviews that rejected his new findings because they contradicted accepted models, drove him to new activities and stimulated more work on the subject. Thus, a rejection of his manuscript on foraminifera thriving under sulphidic conditions, by an international journal ("…anoxic foraminifera don't seem reasonable…"), led him to the book on anoxic strategies in eukaryotes (Altenbach et al. 2012a). In this book we have published together a speculative essay on the relevance of anoxic and agglutinated foraminifera to Archean eukaryote evolution. ...
... The heterotrophic dinofl agellate O . marina encountered in the chemocline of LZC and KS is able to live in the presence of hydrogen sulfi de (Altenbach et al., 2012), which enables that predator to use food resources in the chemocline inaccessible to obligate aerobes. ...
An unusual feature of the saline stratified lakes that were formed due to ongoing postglacial uplift on the White Sea coast is the presence of several differently colored thin layers in the zone with sharp gradients. Colored layers in five lakes at various stages of separation from the sea were investigated using optical microscopy, spectrophotometry, spectrofluorimetry, and photobiology. The upper greenish colored layer located in the aerobic strata of all lakes near the compensation depth of 1% light penetration contains green algae. In the chemocline, another layer, brightly green, red or pink, is dominated by mixotrophic flagellates. Despite the very low light intensities and the presence of H2S, active photosynthesis by these algae appears to be occurring, as indicated by high values of the maximum quantum yield of primary photochemistry, electron transport activity, photosynthetic activity of photosystem II, the fraction of active centers, and low values of heat dissipation. In the reduced zone of the chemocline, a dense green or brown suspension of anoxygenic phototrophs (green sulfur bacteria) is located.
... anoxic-no dissolved oxygen, dysoxic-0.1-1 ml/l; Altenbach et al. 2011;Sen Gupta 1999) bottom-water environments. The combination of foraminiferal records and geochemical proxies allowed us to recognize faunal shifts and their environmental settings and to take a further step in inferring specific biological evolutionary adaptations that enabled benthic foraminifera to successfully colonize anoxic-dysoxic environments, in a similar manner as their modern successors. ...
The ideas summarized in Figs. 1. 1–1. 3 can be expressed with the help of certain aspects of graph theory. This field of applied mathematics provides several useful theorems for overcoming the concrete difficulties so often met in biochronology. In addition, its notation is convenient to describe the algorithms which are used in the UAgraph program
both to explain the structure of difficult biostratigraphic data, and to construct unitary associations and identify them in fossil-bearing beds.
... Here we present new evidence from the Late Cretaceous Levantine high productivity sequence (upper Menuha, Mishash, and lower Ghareb formations), which show that different benthic foraminifera species with diverse morphologies were able to tolerate and successfully colonize anoxic-dysoxic (i.e., anoxic = no dissolved oxygen, dysoxic = 0.1-1 ml/l; Bernhard and Sen Gupta 1999;Altenbach et al. 2012) bottom water environments. This unique depositional environment was investigated using a combination of foraminiferal records and diverse geochemical proxies analyzed in the same samples. ...
Abstract.—It has generally been argued that the majority of fossil benthic foraminifera, the most common proxy for paleo bottom oceanic conditions, could not tolerate anoxia. Here we present evidence that fossil foraminifera were able to successfully colonize anoxic–dysoxic bottom waters, by using adaptations similar to those found in living species. Our study is based on a multi proxy micropaleontological and geochemical investigation of the Upper Cretaceous sediments from the Levant upwelling regime. A shift from buliminid to diverse trochospiral dominated assemblages was recorded in an interval with a distinct anoxic geochemical signature coinciding with a regional change in lithology. This change was triggered by an alteration in the type of primary producers from diatoms to calcareous nannoplankton, possibly causing modifications in benthic foraminiferal morphological and physiological adaptations to life in the absence of oxygen.
Our data show that massive blooms of triserial (buliminid) benthic foraminifera with distinct
apertural and test morphologies during the Campanian were enabled by their ability to sequester diatom chloroplasts and associate with bacteria, in a similar manner as their modern analogs. Diverse trochospiral forms existed during the Maastrichtian by using nitrate instead of oxygen for their respiratory pathways in a denitrifying environment. Species belonging to the Stilostomellidae and Nodosariidae families might have been affected by the change in food type arriving to the seafloor after the phytoplankton turnover at the Campanian/Maastrichtian boundary, in a similar manner as their mid Pleistocene descendants prior to their extinction. This study promotes the need for a re-evaluation of the current models used for interpreting paleoceanographic data and demonstrates that the identification of adaptations and mechanisms involved in promoting sustained life under anoxic to dysoxic conditions should become a standard in faunal paleoceanographic studies.
... Euplotes elegans can reproduce under low oxygen content and survive anaerobically up to 24 h. The enzyme system of O. marina allows it to stay active in the absence of oxygen (Altenbach et al., 2012). Plagiopylidae ciliates can occupy different anoxic habitats including invertebrate internal environments (Fenchel & Finaly, 1990;Lynn & Strüder-Kypke, 2002). ...
Due to postglacial isostatic uplift many stratified lakes, at different stages of isolation, are located along the shores of the White Sea. In five lakes, located near the White Sea Biological Station of Moscow State University, salinity, temperature, pH, concentration of dissolved oxygen, redox potential, and illuminance were measured. Distribution of microorganisms and spectral properties of water layers were also studied. All the lakes had a narrow bright coloured layer in the redox zone caused by mass development of phototropic microorganisms. Light absorption and fluorescence spectra indicated algae containing chlorophyll a predominate in the red water layers while the colouration of green and brown layers is caused by green sulphur bacteria with bacteriochlorophylls d and e. Sunlight is completely absorbed in the redox zone because of the high density of algae and/or bacteria, resulting in aphotic conditions below. Coloured layers act as a specific biotope for special communities of microorganisms. Eukaryotes identified by the 18S rRNA gene included different species of mixotrophic algae and ciliates resistant to anoxia. The water layer colour and spectral characteristics (i.e. light absorption and fluorescence) of water in the redox zone can be considered indicators of the stage of lake isolation from the sea, with the red colour caused by cryptophyte alga
Rhodomonas
sp. bloom found in earlier stages and brown and green colours caused by green sulphur bacteria in later stages.
The proliferation of marine algae in the Neoproterozoic Era is thought to have stimulated the ecology of predatory microbial eukaryotes. To test this proposal, we introduced algal particulate matter (APM) to marine sediments underlying a modern marine oxygen minimum zone with bottom-water oxygen concentrations approximating those of the late Neoproterozoic water column. We found that under anoxia, APM significantly stimulated microbial eukaryote gene expression, particularly genes involved in anaerobic energy metabolism and phagocytosis, and increased the relative abundance of 18 S rRNA from known predatory clades. We additionally confirmed that APM promoted the reproduction of benthic foraminifera under anoxia with higher-than-expected net growth efficiencies. Overall, our findings suggest that algal biomass exported to the Neoproterozoic benthos stimulated the ecology of benthic predatory protists under anoxia, thereby creating more modern food webs by enhancing the transfer of fixed carbon and energy to eukaryotes occupying higher trophic levels, including the earliest benthic metazoans.
The Southeast Pacific arid zone, encompassing Peruvian and Chilean coastal deserts, features several wetlands that are influenced by upwelling waters and provide critical ecosystem services. Despite the significance of wetlands such as the coastal lagoon Poza La Arenilla (PLA) in Lima, Peru, their proximity to urban areas exposes them to eutrophication. This, in turn, presents considerable challenges for conservation efforts. Effective conservation strategies demand a comprehensive assessment of trophic conditions, achieved here by studying living and dead benthic foraminifera assemblages. These microorganisms serve as bioindicators for organic sources and enrichment. We explored their relationships with hydrological factors (dissolved oxygen, temperature, salinity) and sedimentary parameters (total organic matter, carbon, nitrogen, stable isotopes) in the PLA. Our results show that foraminifera distribution is influenced by organic matter (OM) from marine phytoplankton/algae and bacterial sources. Foraminifera were dominated by hyaline and soft-walled species, and 4 distinct foraminiferal assemblages were identified. Psammophaga sp1 prevailed in areas with abundant OM, while Bathysiphon sp. was associated with less organic conditions in sandy sediments. Additionally, Quinqueloculina seminulum , Buliminella elegantissima , Ammonia confertitesta , and Bathysiphon sp. were frequent and abundant species in the PLA. Dead assemblages showed a 2-fold increase in species richness compared to living foraminifera, indicating seasonal species turnover. Our study evidenced the importance of the whole diversity of foraminifera for environmental and/or ecological assessments, as groups of soft-walled and agglutinated foraminifera comprise potential bioindicators for eutrophication.
Based on molecular and morphological characters, we describe a new species of monothalamous
foraminifera, Psammophaga secriensia sp. nov., that was sampled from two coastal locations
(48 m and 53 m depth) on the Romanian Black Sea continental shelf. Molecular data further confirm
its presence in the northeastern part of the Black Sea (Balaklava Bay, 5–10 m depth). Specimens
of Psammophaga secriensia sp. nov. are characterized by an elongate to broadly pyriform test and
a simple rounded aperture. The wall is translucent and the cytoplasm contains mineral grains of
different sizes. The genus Psammophaga, including Psammophaga simplora and several undetermined
morphotypes, has been reported from different areas of the Black Sea. Previous research using an
integrative taxonomic approach has identified two additional species (Psammophaga zirconia; Psammophaga
sp., Gooday et al., 2011) occurring in the Black Sea. Monothalamids are an important part of
the meiobenthos in the Black Sea and our results increase the knowledge of foraminiferal diversity in
this marginal sea.
High input of organic carbon and/or slowly renewing bottom waters frequently create periods with low dissolved oxygen concentrations on continental shelves and in coastal areas; such events can have strong impacts on benthic ecosystems. Among the meiofauna living in these environments, benthic foraminifera are often the most tolerant to low oxygen levels. Indeed, some species are able to survive complete anoxia for weeks to months. One known mechanism for this, observed in several species, is denitrification. For other species, a state of highly reduced metabolism, essentially a state of dormancy, has been proposed but never demonstrated. Here, we combined a 4 weeks feeding experiment, using ¹³C-enriched diatom biofilm, with correlated TEM and NanoSIMS imaging, plus bulk analysis of concentration and stable carbon isotopic composition of total organic matter and individual fatty acids, to study metabolic differences in the intertidal species Ammonia tepida exposed to oxic and anoxic conditions. Strongly contrasting cellular-level dynamics of ingestion and transfer of the ingested biofilm components were observed between the two conditions. Under oxic conditions, within a few days, intact diatoms were ingested, degraded, and their components assimilated, in part for biosynthesis of different cellular components: ¹³C-labeled lipid droplets formed after a few days and were subsequently lost (partially) through respiration. In contrast, in anoxia, fewer diatoms were initially ingested and these were not assimilated or metabolized further, but remained visible within the foraminiferal cytoplasm even after 4 weeks. Under oxic conditions, compound specific ¹³C analyses showed substantial de novo synthesis by the foraminifera of specific polyunsaturated fatty acids (PUFAs), such as 20:4(n-6). Very limited PUFA synthesis was observed under anoxia. Together, our results show that anoxia induced a greatly reduced rate of heterotrophic metabolism in Ammonia tepida on a time scale of less than 24 hours, these observations are consistent with a state of dormancy.
Background
Insects are renowned for their ability to survive anoxia. Anoxia tolerance may be enhanced during chilling through metabolic suppression. AimsHere, the metabolomic response of insects to anoxia, both with and without chilling, for different durations (12–36 h) was examined to assess the potential cross-tolerance mechanisms. ResultsChilling during anoxia (cold anoxia) significantly improved survival relative to anoxia at warmer temperatures. Reduced intermediate metabolites and increased lactic acid, indicating a switch to anaerobic metabolism, were characteristic of larvae in anoxia. Conclusions
Anoxia tolerance was correlated survival improvements after cold anoxia were correlated with a reduction in anaerobic metabolism.
Here we present a record of size-normalized shell weight for four species of benthic foraminifera through a period of rapid environmental change during the most recent deglaciation (Santa Barbara Basin, CA). A strong Oxygen Minimum Zone (OMZ), the product of high surface productivity and poor ventilation, characterizes the eastern Pacific; this subsurface zone is mechanistically coupled with high concentrations of dissolved inorganic carbon. The OMZ migrated vertically during warming of the last deglaciation, leading to rapid shifts in the oxygenation and inorganic carbon system of the benthos. The size-normalized weight (SNW) of benthic foraminifers Uvigerina peregrina, Bolivina interjuncta, and Bolivina tumida reflects only the broad trends of the vertical migration of the OMZ, and inorganic carbon system, overshadowed by clear species-specific trends. The relative importance of OMZ migrations versus other environmental variables and optimal growth conditions differs across species of benthic foraminifera. In U. peregrina, SNW primarily peaks with foraminiferal density and increased abundance of that species, while B. interjuncta and B. tumida increase in SNW with a shrinking of the OMZ (and carbon maximum) in the late Holocene. Bolivina argentea shows no long-term trends in SNW potentially due to its ability to migrate through the sediment. Our results suggest that, while inorganic carbon and dissolved oxygen may play a role in determining shell weight across species of benthic foraminifera, neither parameter alone is responsible for changes in benthic foraminiferal shell weight in the fossil record.
Life exists in almost every ecological niche on Earth, and the majority of living organisms thrive in “normal” or “common” conditions. These are the environments that we are familiar with from our daily life. The organisms distributed under those conditions are at moderate temperature (5 to ~40 °C), 1 atm sea level pressure, with our known gas compositions, and oxygen rich atmosphere, close to neutral pH level. We consider these conditions as benign ambient habitats.
The detailed analyses of recent epibionthic foraminifera Cibicides lobatulus from the Barents Sea as well as their Cretaceous morphological counterparts (asymmetric and low trochospiral benthic forms) suggest that large pores are diagnostic for the adhesive side of the tests of some epibenthic species. The pores seem to provide organic outgrowths which are attached to the hard substrate and stabilise the test in the sedimentary environment. The occurrence of asymmetrical test and coarse pores on only one side of the foraminiferal test seems therefore to be indicative of an epifaunal mode of life, while a symmetrical test and bilateral coarse porosity suggests living within the sediment.
Fifty two surface sediment samples collected from the region off Goa, central west coast of India from water depths of 15–3300 m were analyzed with special emphasis on foraminiferal content. Rectilinear benthic foraminiferal morphogroup shows a high relative abundance within Oxygen Minimum Zone (OMZ), both shallow marine (50–60 m water depth) and intermediate to deep water (150–1500 m water depth). We gave special emphasis on four rectilinear foraminiferal genera, namely Fursenkoina, Bolivina, Bulimina and Uvigerina to observe their individual distribution among OMZ. We found genus Fursenkoina predominates at the shallow water OMZ, within the water depth zone of 50–60 m. Within 150–1500 m water depth, which is considered as intermediate to deep water OMZ in this region, genus Uvigerina shows its highest abundance above 1000 m water depth, whereas genus Bulimina shows its affinity with deeper water environment (>1000 m water depth). Genus Bolivina does not show any such depth preference, except its higher abundance in only intermediate to deep water OMZ. This depth differentiation among four rectilinear benthic foraminiferal genera presents the basic data for palaeoclimatic study based on the extent and intensity of OMZ along with the palaeobathymetry study.
Anoxia was successfully induced in four benthic chambers installed at 24m depth on the northern Adriatic
seafloor from 9 days to 10 months. To accurately determine whether benthic foraminifera can survive experimentally induced prolonged anoxia, the CellTracker™ Green method was applied and calcareous and agglutinated foraminifera were analyzed. Numerous individuals were found living at all sampling times and at all sampling depths (to 5 cm), supported by a ribosomal RNA analysis that revealed that certain
benthic foraminifera were active after 10 months of anoxia. The results show that benthic foraminifera can survive up to 10 months of anoxia with co-occurring hydrogen sulfides. However, foraminiferal standing stocks decrease with sampling time in an irregular manner. A large difference in standing stock between two cores sampled under initial conditions indicates the presence of a large spatial heterogeneity of the foraminiferal faunas. An unexpected increase in standing stocks after one month is tentatively interpreted as a reaction to increased food availability due to the massive mortality of infaunal macrofaunal organisms. After this, standing stocks decrease again in cores sampled after 2 months of anoxia to then attain a minimum in the cores sampled after 10 months. We speculate that the trend of overall decrease of standing
stocks is not due to the adverse effects of anoxia and hydrogen sulfides but rather due to a continuous diminution of labile organic matter.
SUMMARY Magnetotactic bacteria (MTB) are widespread, motile, diverse prokaryotes that biomineralize a unique organelle called the magnetosome. Magnetosomes consist of a nano-sized crystal of a magnetic iron mineral that is enveloped by a lipid bilayer membrane. In cells of almost all MTB, magnetosomes are organized as a well-ordered chain. The magnetosome chain causes the cell to behave like a motile, miniature compass needle where the cell aligns and swims parallel to magnetic field lines. MTB are found in almost all types of aquatic environments, where they can account for an important part of the bacterial biomass. The genes responsible for magnetosome biomineralization are organized as clusters in the genomes of MTB, in some as a magnetosome genomic island. The functions of a number of magnetosome genes and their associated proteins in magnetosome synthesis and construction of the magnetosome chain have now been elucidated. The origin of magnetotaxis appears to be monophyletic; that is, it developed in a common ancestor to all MTB, although horizontal gene transfer of magnetosome genes also appears to play a role in their distribution. The purpose of this review, based on recent progress in this field, is focused on the diversity and the ecology of the MTB and also the evolution and transfer of the molecular determinants involved in magnetosome formation.
Synthetic life: The origin of life on the early Earth, and the ex novo transition of non-living matter to artificial living systems are deep scientific challenges that provide a context for the development of new chemistries with unknown technological consequences. This Essay attempts to re-frame some of the epistemological difficulties associated with these questions into an integrative framework of proto-life science. Chemistry is at the heart of this endeavour.
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