Carbon and nitrogen uptake through photosynthesis and feeding by photosymbiotic Acantharia

Abstract

Background: Mixotrophy, combining phagotrophy and photoautotrophy in order to acquire nutrients and energy, is a widespread trophic mode in marine protist plankton. Acantharia (Radiolaria) are ubiquitous, but still uncultured oceanic protists. Many of them are mixoplanktic by endosymbiotic relations with microalgae. Here we aimed at quantitatively assessing phototrophy (inorganic nutrients) and phagotrophy (organic nutrients) of photosymbiotic Acantharia, to understand their physiology, and thereby improve integrations of mixotrophy into ecological models of oceanic ecosystems. Methods: Freshly collected Acantharia were incubated with stable isotopes of inorganic carbon and nitrogen to determine photosynthetic uptake rates. Grazing experiments (prey disappearance) were done with different algal cultures as potential food organisms to measure the contribution of prey ingestion to the acantharian metabolism. Fluorescently (and isotopically) labelled prey was used to verify prey uptake, qualitatively. Results/Conclusions: Carbon uptake rates were unaffected by the nitrogen source (i.e., nitrate or ammonium). Total carbon inorganic uptake rate was 1112±82 pgC h-1 Acantharia‑1, 22.3±1.6 pgC h-1 symbiont cell-1assuming 50 symbionts per Acantharia, at ~155-μmol photons m−2 s−1 irradiance. The Acantharia studied could use both inorganic ammonium and nitrate, but ammonium was taken up at a ~5 times higher rate. Prey ingestion of the haptophyte, Isochrysis galbana, was detected using labelled algae. Significant grazing by Acantharia could only be established on the dinoflagellate Effrenium voratum, with a grazing rate of 728 prey Acantharia‑1 hour-1 (i.e., ~56.3 ngC h-1, 46% of total holobiont carbon content) at a ratio of 1.06x104 prey predator-1. Daily photosynthetic carbon uptake rates made up ~14.5% of the total holobiont carbon content (0.9% hourly). The extent to which photosynthates are used and assimilated by the acantharian cell and/or if it is used for catabolic processes to obtain energy is still to be studied. Isotopic ratios further suggests seasonal differences in the usage of each trophic mode.