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

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.