Foraminiferal Metabolism Under Hypoxia: Sub-Cellular NanoSIMS Imaging of Intertidal Ammonia tepida Feeding Behavior

Charlotte LeKieffre, Ecole Polytechnique Fédérale de Lausanne Lausanne, Switzerland, Lausanne, Switzerland, Jorge Spangenberg, Institute of Earth Surface Dynamics, University of Lausanne, Switzerland, Lausanne, Switzerland, Emmanuelle Geslin, Université d’Angers, France, France and Anders Meibom, Swiss Federal Institute of Technology Lausanne, Lausanne, Switzerland
Abstract:
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.

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