Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts

Abstract

The symbiotic planktonic foraminiferaOrbulina universainhabits open ocean oligotrophic ecosystems where dissolved nutrients are scarce and often limit biological productivity. It has previously been proposed thatO. universameets its nitrogen (N) requirements by preying on zooplankton, and that its symbiotic dinoflagellates recycle metabolic ‘waste ammonium’ for their N pool. However, these conclusions were derived from bulk15N-enrichment experiments and model calculations, and our understanding of N assimilation and exchange between the foraminifer host cell and its symbiotic dinoflagellates remains poorly constrained. Here, we present data from pulse-chase experiments with13C-enriched inorganic carbon,15N-nitrate, and15N-ammonium, as well as a13C- and15N- enriched heterotrophic food source, followed by TEM (transmission electron microscopy) coupled to NanoSIMS (nanoscale secondary ion mass spectrometry) isotopic imaging to visualize and quantify C and N assimilation and translocation in the symbiotic system. High levels of15N-labelling were observed in the dinoflagellates and in foraminiferal organelles and cytoplasm after incubation with15N-ammonium, indicating efficient ammonium assimilation. Only weak15N-assimilation was observed after incubation with15N-nitrate. Feeding foraminifers with13C- and15N-labelled food resulted in dinoflagellates that were labelled with15N, thereby confirming the transfer of15N-compounds from the digestive vacuoles of the foraminifer to the symbiotic dinoflagellates, likely through recycling of ammonium. These observations are important for N isotope-based palaeoceanographic reconstructions, as they show that δ15N values recorded in the organic matrix in symbiotic species likely reflect ammonium recycling rather than alternative N sources, such as nitrates.