Symbiodiniaceae Are the First Site of Heterotrophic Nitrogen Assimilation in Reef-Building Corals

Coral reefs depend on the highly optimized mutualistic relationship between corals and Symbiodiniaceae dinoflagellates. Both partners exchange nutrients obtained through heterotrophy of the host and autotrophy of the symbionts. While heterotrophy helps corals withstand the harmful effects of seawater warming, the exchange of heterotrophic nutrients between the two partners is poorly understood. Here, we used compound-specific δ(15)N and δ(13)C of amino acids (δ(15)N(AA) and δ(13)C(AA)) and a (15)N pulse-chase experiment with Artemia salina nauplii in two coral-dinoflagellate associations to trace the assimilation and allocation of heterotrophic nutrients within the partners. We observed that changes in the trophic position (TP(Glx-Phe)), δ(15)N(AA), and δ(13)C(AA) with heterotrophy were holobiont-dependent. Furthermore, while TP(Glx-Phe) and δ(15)N of all AAs significantly increased with heterotrophy in the symbionts and host of Stylophora pistillata, only the δ(15)N(AA) of the symbionts changed in Turbinaria reniformis. Together with the pulse-chase experiment, the results suggested a direct transfer of heterotrophically acquired AAs to the symbionts of S. pistillata and a transfer of ammonium to the symbionts of T. reniformis. Overall, we demonstrated that heterotrophy underpinned the nutrition of Symbiodinaceae and possibly influenced their stress tolerance under changing environmental conditions.