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

Charlotte Lekieffre,Haojia Ren,Jennifer S Fehrenbacher,Ann D Russell,Emmanuelle Geslin,Howard J Spero,Anders Meibom

doi:10.1098/rspb.2020.0620

Abstract

The symbiotic planktonic foraminifera Orbulina universa inhabits open ocean oligotrophic ecosystems where dissolved nutrients are scarce and often limit biological productivity. It has previously been proposed that O. universa meets 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 bulk 15N-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 with 13C-enriched inorganic carbon, 15N-nitrate, and 15N-ammonium, as well as a 13C- and 15N- 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 of 15N-labelling were observed in the dinoflagellates and in foraminiferal organelles and cytoplasm after incubation with 15N-ammonium, indicating efficient ammonium assimilation. Only weak 15N-assimilation was observed after incubation with 15N-nitrate. Feeding foraminifers with 13C- and 15N-labelled food resulted in dinoflagellates that were labelled with 15N, thereby confirming the transfer of 15N-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.

Highlights

Planktonic foraminifera are important contributors to primary production in open ocean oligotrophic environments because they are often associated with large populations of photosynthesizing symbiotic algae such as dinoflagellates [1,2]
When nitrate is not limiting in the environment, model calculations revealed that up to 57% of the foraminiferal N could be translocated from the symbionts, and even up to 90– 100% for model calculations taking into account nitrogen uptake by the symbionts from the recycled ammonium pool
Our data show that ammonium is the major source of N used for protein and nuclear synthesis by the symbiotic dinoflagellates in the planktonic foraminifera Orbulina universa

Summary

Introduction

Planktonic foraminifera are important contributors to primary production in open ocean oligotrophic environments because they are often associated with large populations of photosynthesizing symbiotic algae such as dinoflagellates [1,2]. Several studies have concluded that symbiont-bearing foraminifera must meet their nitrogen requirements via capture and assimilation of zooplankton prey N, because the concentrations and diffusion rates of dissolved ammonium or nitrate are insufficient to explain their growth rate. In this regard, δ13C values measured on different amino acids from the symbiotic species Orbulina universa are consistent with two isotopically distinct sources of carbon and nitrogen, isotopically heavy metabolic carbon and nitrogen from its symbionts and relatively lighter carbon and nitrogen from the diet [6,7]. It is likely that planktonic foraminifer can assimilate inorganic nitrogen from seawater if it is available [2,5,8] because ammonium assimilation has already been reported in a benthic species with inactive kleptoplasts [9]

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