The stoichiometry of coral-dinoflagellate symbiosis: carbon and nitrogen cycles are balanced in the recycling and double translocation system

Symbioses between microalgae and animal hosts have the advantage of acquiring and sharing autotrophically produced organic carbon (C) as their energy source. However, the stoichiometry and turnover rates of biological elements in symbioses are not fully understood because of complicated metabolic interactions. We report the first comprehensive and simultaneous measurement of C and nitrogen (N) flows through coral–dinoflagellate symbiosis by using the unique approach of dual-isotope labeling with 13C and 15N, in situ chasing, and isotope-mixing models. The coral autotrophy occurred with much lower C:N ratios than previously thought, and the autotrophically produced N-rich organic matter was efficiently transferred to the animal host through two different pathways. In contrast to the dynamic N cycles within the symbiosis, the N uptake from the ambient seawater was extremely limited, which enabled the coral symbiosis to sustain N with a long turnover time (1 year). These findings suggest that coral endosymbionts are not under N limitation but are actively producing organic N and driving microscale N cycles in the reef ecosystem. The present techniques could be applied to further quantify the C and N cycles in other symbiotic interactions and reveal their ecological advantages.