13C metabolomics reveals widespread change in carbon fate during coral bleaching

Introduction Rising seawater temperatures are threatening the persistence of coral reefs; where above critical thresholds, thermal stress results in a breakdown of the coral-dinoflagellate symbiosis and the loss of algal symbionts (coral bleaching). As symbiont-derived organic products typically form a major portion of host energy budgets, this has major implications for the fitness and persistence of symbiotic corals. Objectives We aimed to determine change in autotrophic carbon fate within individual compounds and downstream metabolic pathways in a coral symbiosis exposed to varying degrees of thermal stress and bleaching. Methods We applied gas chromatography-mass spectrometry coupled to a stable isotope tracer (C-13), to track change in autotrophic carbon fate, in symbiont and host individually, following exposure to elevated water temperature. Results Thermal stress resulted in partner-specific changes in carbon fate, which progressed with heat stress duration. We detected modifications to carbohydrate and fatty acid metabolism, lipogenesis, and homeostatic responses to thermal, oxidative and osmotic stress. Despite pronounced photodamage, remaining in hospite symbionts continued to produce organic products de novo and translocate to the coral host. However as bleaching progressed, we observed minimal C-13 enrichment of symbiont long-chain fatty acids, also reflected in C-13 enrichment of host fatty acid pools. Conclusion These data have major implications for our understanding of coral symbiosis function during bleaching. Our findings suggest that during early stage bleaching, remaining symbionts continue to effectively translocate a variety of organic products to the host, however under prolonged thermal stress there is likely a reduction in the quality of these products.