A benthic foraminifera species respond to anoxia with a strong metabolic shift suggesting a state of dormancy

Emmanuelle Geslin, Charlotte Madeleine Nicole Lekieffre, Anders Meibom
2016
Poster talk

Abstract

Low-oxygenation events are more and more frequent and strong on continental shelves and in coastal areas where renewal of bottom waters is slow. Among the meiofauna living in such environments, foraminifera are among the most tolerant to the lack of oxygen. Some benthic foraminiferal species are able to survive hypoxia, and even anoxia, for weeks to months. Different species must have developed different mechanisms for survival - hypotheses include reduction of the metabolism, symbiosis with bacteria, or denitrification. Ammonia tepida, one of the most abundant species in intertidal environments, is able to survive up to 60 days in anoxia. Here we combined a 4 week feeding experiment using 13C-enriched microalgae (diatoms), with correlated transmission electron microscopy (TEM) and NanoSIMS (Secondary Ion Mass Spectrometry) imaging, and concentrations (GC/MS, GC/FFID), as well as bulk and compound specific carbon isotope ratios (13C/12C obtained by EA/IRMS and GC/C/IRMS) of individual fatty acids (FAs) to study the metabolic differences in intertidal Ammonia tepida exposed to oxic and anoxia conditions, respectively. Strongly contrasting cellular-level dynamics of integration and transfer of the ingested biofilm components were observed under the two conditions. Under oxic conditions, within a few days, intact diatoms (i.e. including the frustule) were ingested, assimilated and consumed, in part for biosynthesis of different cellular components: 13C-labeled lipid droplets formed over a timescale of a few days and were then partly lost 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. The compound specific 13C/12C ratios indicated substantial de novo synthesis by the foraminifera of polyunsaturated FAs (PUFAs), such as 20:4(n-6), in oxic conditions; very limited PUFA synthesis was observed under anoxia. Together, our results indicate that anoxia induced a greatly reduced rate of heterotrophic metabolism in Ammonia tepida on a time scale of about 24 hours, which seems consistent with a state of dormancy.

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Emmanuelle Geslin, Charlotte Madeleine Nicole Lekieffre, Anders Meibom
2016
Poster talk

Abstract

Official source

https://infoscience.epfl.ch/record/224526?ln=en

About this result

Related concepts (22)

Related concepts

Related publications (64)

Related publications

Dormant or not dormant? Benthic foraminiferal metabolism under anoxia

Emmanuelle Geslin, Charlotte Madeleine Nicole Lekieffre, Anders Meibom

Hypoxic events particularly affect benthic ecosystems on continental shelves and in coastal areas where renewal of bottom waters slow. Foraminifera living in such environments are among the most tolerant to hypoxia in the meiofauna. Some foraminifera species are able to survive hypoxia, and even anoxia, for weeks to months. Different species must have developed different mechanisms for survival - hypotheses include reduction of the metabolism, symbiosis with bacteria, or denitrification. NanoSIMS (Secondary Ion Mass Spectrometry) imaging is a powerful analytical technique to visualize and quantify the incorporation and transfer of isotopically labeled compounds in organisms with subcellular resolution. We used NanoSIMS imaging, correlated with TEM ultrastructural observations of individual foraminifera, to study the metabolism of intertidal Ammonia tepida, which has shown strongly reduced metabolism under anoxia. Individuals were fed with a 13C-labeled microalgal biofilm and incubated for 4 weeks in oxic and anoxic conditions, respectively. NanoSIMS imaging reveal strongly contrasting cellular-level dynamics of integration and transfer of the ingested biofilm components under the two conditions. In oxic conditions, ingested biofilm components are internalized, metabolized, and used for biosynthesis of different cellular components on a time scale of 24 hours: Lipid droplets are formed, then consumed through respiration. In contrast, upon the onset of anoxia, individual internalized biofilm components remain visible within the cytoplasm after 4 weeks. Lipids of different compositions are initially formed but then not respired. These observations indicate that foraminifera do initially have an active heterotrophic metabolism in the absence of oxygen, but this it is strongly reduced when oxygen is no longer available. Isotopic labeling experiments, NanoSIMS and TEM imaging, and GC-MS will be key to study metabolic mechanisms under anoxic conditions in marine environments.

2016

Surviving anoxia in marine sediments: The metabolic response of ubiquitous benthic foraminifera (Ammonia tepida)

Stéphane Laurent Escrig, Emmanuelle Geslin, Charlotte Madeleine Nicole Lekieffre, Anders Meibom

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 C-13-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: C-13-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 C-13 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.

Public Library of Science2017

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More and more marine areas are subjected to depleted-O2 concentration, mainly due to eutrophication induced by human activities. These phenomena affect benthic ecosystems, in particular continental shelves and coastal areas where the renewal of the bottom waters is low and/or the organic matter flux is high. Some species of benthic foraminifera are resistant to this hypoxic/anoxic events, surviving weeks to months without oxygen. One of the species known to survive to such extreme condition is the benthic one Ammonia tepida. However the metabolic process by which it succeed in it remains unknown. One hypothesis is that this species would be able to lower its metabolism under oxygen depleted conditions, until the return of better conditions. The aim of the present study is to understand the feeding behaviors of A. tepida under anoxia. For this purpose a laboratory experiment involving incubation with living A. tepida was carried out under controlled oxygen concentrations. The individuals were fed with a pulse of 13C-labeled diatoms (Navicula sp.) and then incubate in oxic or anoxic conditions during 28 days. Along the incubation time, observation of the cell ultrastructure with Transmission Electronic Microscope (TEM) and detection in the cell of the isotopic 13C signal using nanoSIMS, were made. The nanoSIMS (nanoscale Secondary-Ion Mass Spectrometry) is an analytical technique that allows to visualize the incorporation and transfer of isotopically labeled compounds in organisms; thus in our case to follow the ingestion of labeled-diatoms and further transfer of carbon in the cytoplasm of the foraminifera. According to the results acquired in this study, in both conditions the foraminifera directly integrate the diatoms in their cytoplasm during the first hours of the incubation. Then, in oxic conditions, these diatoms are quickly fully degraded, within 3 days, and the 13C-labeled compounds are transferred in the organelles of the cytoplasm. Whereas in anoxia, only a fraction of the diatoms are degraded and the transfer to the foraminifera cytoplasm is weak. These results are confirmed by the δ13C of the foraminifera, measured in bulk by mass spectrometry (GC-MS). In anoxia the δ13C is slightly increasing the first 24h, meaning that the 13C content of the cell increased, and then it remains stable until the end of the experiment. This leads us to assume that the foraminifera stop, or at least strongly lower their metabolic rate under anoxic condition.

2015

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