Abstract
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.
Highlights
Benthic foraminifera are eukaryote unicellular protists and ubiquitous in marine sediments from shallow water estuaries to the deep ocean [1]
At Day 7, the total organic carbon (TOC) had dropped to 0.8 ±0.1 μg C×ind-1 and this level was maintained for the rest of the experiment (p>0.05) (Fig 1A)
Benthic foraminifera Ammonia tepida are ubiquitous in coastal marine sediments, where they are often exposed to hypoxia or completely anoxic conditions
Summary
Benthic foraminifera are eukaryote unicellular protists and ubiquitous in marine sediments from shallow water estuaries to the deep ocean [1]. Hypoxic and anoxic events strongly and more frequently affect benthic ecosystems, in particular on continental shelves and in coastal areas where renewal of bottom water is slow and/or organic input is high [16,17,18]. Even during periods with normal oxic conditions in bottom waters, foraminifera and other benthic meiofauna species can be (and frequently are) exposed to low O2 levels because bioturbation mechanically moves them deeper into the sediments [43,44]. A. tepida is regularly found alive at depths of 4 to 26 cm, i.e. below the O2 penetration depth, as a result of bioturbation [46,47] These observations raise questions about the mechanism(s) that enable foraminifera to survive sudden changes to anoxia, often for extended periods of time
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