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

Abstract

ABSTRACT 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 δ15N and δ13C of amino acids (δ15NAA and δ13CAA) and a 15N 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 (TPGlx-Phe), δ15NAA, and δ13CAA with heterotrophy were holobiont-dependent. Furthermore, while TPGlx-Phe and δ15N of all AAs significantly increased with heterotrophy in the symbionts and host of Stylophora pistillata, only the δ15NAA 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. IMPORTANCE Coral reefs rely upon the highly optimized nutritional symbiosis between corals and Symbiodiniaceae dinoflagellates. Heterotrophic feeding on plankton is key to the resistance of corals to environmental stress. Yet, a detailed understanding of heterotrophic nutrient assimilation and utilization within the symbiosis is lacking. Here, we used the advanced tools of compound-specific isotope analysis of amino acids and 15N-labeling of plankton to show that heterotrophy underpinned the nutrition of Symbiodinaceae. Symbionts received either heterotrophically acquired amino acids or recycled ammonium due to their association with the coral host. This study brought new insight into the nutrient exchanges in coral-Symbiodiniaceae associations and allowed a better understanding of the mechanisms involved in coral resistance to environmental stress.

Keywords

• pulse-chase
• stable isotopes
• coral reefs
• nitrogen
• Symbiodiniaceae
• compound-specific isotope analysis of amino acids