Coupled carbon and nitrogen cycling regulates the cnidarian-algal symbiosis

Efficient nutrient recycling underpins the ecological success of the cnidarian-algal symbiosis in oligotrophic waters that forms the basis of coral reef ecosystems. In a stable symbiosis, nitrogen limitation restricts the growth of algal endosymbionts and stimulates their release of photosynthates to the cnidarian animal host. However, the detailed mechanisms controlling nitrogen availability in hospite and their role in symbiosis regulation remain poorly understood. Here, we studied the metabolic regulation of symbiotic nitrogen cycling in the sea anemone Aiptasia by experimentally altering labile carbon availability in a series of experiments. Using isotope labeling experiments and NanoSIMS imaging, we show that the competition for environmental ammonium between the host and its algal symbionts is regulated by carbon availability. Light regimes that were optimal for algal photosynthesis increased carbon availability in the holobiont and enhanced symbiotic competition for nitrogen. Consequently, algal symbiont densities were lowest under optimal environmental conditions and increased toward the tolerance limits of the symbiosis. This metabolic regulation promotes efficient carbon recycling in a stable symbiosis across a wide range of environmental conditions. At the same time, the dependence on resource competition can favor parasitic interactions that may explain the instability of the symbiosis as the environmental conditions in the Anthropocene shift towards its tolerance limits.