Subcellular investigation of photosynthesis-driven carbon and nitrogen assimilation and utilization in the symbiotic reef coral Pocillopora damicornis

Background: Shallow water reef building scleractinian corals form essential mutualistic endosymbiotic associations with photosynthetic Symbiodinium dinoflagellates. The dinoflagellate endosymbionts provide their animal host partner with photosynthetically derived nutrients that allow the coral to thrive in oligotrophic waters. However little is known about the dynamics of these symbiotic nutritional interactions at the (sub )cellular level. Here we combined nano scale secondary ion mass spectrometry (NanoSIMS) and transmission electron microscopy (TEM) imaging with pulse chase dual isotopic labeling using [13C]bicarbonate and [15N]nitrate to visualize and quantify in situ at submicrometer spatial resolution the dynamics of carbon and nitrogen fluxes between the dinoflagellate endosymbionts and the coral host cells in the tropical reef builder Pocillopora damicornis. Results: Among our main results we observe that (i) through light driven photosynthesis dinoflagellates rapidly assimilate inorganic bicarbonate and nitrate temporarily storing carbon within lipid droplets and starch grains along with carbon and nitrogen incorporation into others cell compartments (ii) the turnover of dinoflagellate carbon reserves strongly relates to the diurnal light cycle (iii) all four cellular layers composing the coral tissue benefit from the translocation of carbon and nitrogen by dinoflagellates (iv) translocated carbon containing photosynthates are rapidly within 15 min translocated to the coral tissue where they preferentially accumulate within coral lipid droplets and glycogen granules whereas nitrogen translocation is delayed by about 3 to 6 hours. Conclusions: Our results provide detailed in situ visualization of the fate of photosynthesis derived carbon and nitrogen in the coral dinoflagellate endosymbiosis and offer a new baseline from which more detailed C and N budgets of reef corals might be constructed.