The Assimilation of Diazotroph-Derived Nitrogen by Scleractinian Corals Depends on Their Metabolic Status

ABSTRACT Tropical corals are associated with a diverse community of dinitrogen (N2)-fixing prokaryotes (diazotrophs) providing the coral an additional source of bioavailable nitrogen (N) in oligotrophic waters. The overall activity of these diazotrophs changes depending on the current environmental conditions, but to what extent it affects the assimilation of diazotroph-derived N (DDN) by corals is still unknown. Here, in a series of 15N2 tracer experiments, we directly quantified DDN assimilation by scleractinian corals from the Red Sea exposed to different environmental conditions. We show that DDN assimilation strongly varied with the corals’ metabolic status or with phosphate availability in the water. The very autotrophic shallow-water (~5 m) corals showed low or no DDN assimilation, which significantly increased under elevated phosphate availability (3 µM). Corals that depended more on heterotrophy (i.e., bleached and deep-water [~45 m] corals) assimilated significantly more DDN, which contributed up to 15% of the corals’ N demand (compared to 1% in shallow corals). Furthermore, we demonstrate that a substantial part of the DDN assimilated by deep corals was likely obtained from heterotrophic feeding on fixed N compounds and/or diazotrophic cells in the mucus. Conversely, in shallow corals, the net release of mucus, rich in organic carbon compounds, likely enhanced diazotroph abundance and activity and thereby the release of fixed N to the pelagic and benthic reef community. Overall, our results suggest that DDN assimilation by corals varies according to the environmental conditions and is likely linked to the capacity of the coral to acquire nutrients from seawater. IMPORTANCE Tropical corals are associated with specialized bacteria (i.e., diazotrophs) able to transform dinitrogen (N2) gas into a bioavailable form of nitrogen, but how much of this diazotroph-derived nitrogen (DDN) is assimilated by corals under different environmental conditions is still unknown. Here, we used 15N2 labeling to trace the fate of DDN within the coral symbiosis. We show that DDN is assimilated by both the animal host and the endosymbiotic algae. In addition, the amount of assimilated DDN was significantly greater in mesophotic, bleached, or phosphorus-enriched corals than in surface corals, which almost did not take up this nitrogen form. DDN can thus be of particular importance for the nutrient budget of corals whenever they are limited by the availability of other forms of dissolved nutrients. Tropical corals are associated with specialized bacteria (i.e., diazotrophs) able to transform dinitrogen (N2) gas into a bioavailable form of nitrogen, but how much of this diazotroph-derived nitrogen (DDN) is assimilated by corals under different environmental conditions is still unknown. Here, we used 15N2 labeling to trace the fate of DDN within the coral symbiosis. We show that DDN is assimilated by both the animal host and the endosymbiotic algae. In addition, the amount of assimilated DDN was significantly greater in mesophotic, bleached, or phosphorus-enriched corals than in surface corals, which almost did not take up this nitrogen form. DDN can thus be of particular importance for the nutrient budget of corals whenever they are limited by the availability of other forms of dissolved nutrients.