Chilling injury to algal symbionts induces host starvation and metabolic reorganization in a temperate cnidarian

Summary Global temperature anomalies increasingly disrupt the cnidarian-algal symbiosis through a phenomenon coined bleaching. In contrast to heat stress, the mechanisms underlying symbiotic breakdown under cold stress remain largely unknown. Combining physiological and metabolomic measurements, we investigated the response of the photosymbiotic sea anemone holobiont Aiptasia couchii to an experiment mimicking a cold spell in the Mediterranean Sea. Within four weeks, we observed the onset of symbiotic breakdown reflected in reduced algal endosymbiont density and chlorophyll a content. While photosynthetic efficiency remained largely unaffected, no gross photosynthesis was detectable in cold-stressed anemones and decreases in glycosyldiacylglycerols and fatty acyl glycosides indicated chloroplast lipid remobilization. This breakdown of symbiotic carbon cycling was reflected in increased dipeptide and ceramide levels suggesting anemones catabolized protein reserves and induced pre-apoptotic pathways. Taken together, these responses suggest a decoupling of light and dark reactions of photosynthesis in cold-stressed endosymbionts, resembling chilling injury in higher plants and free-living microalgae. This chilling-induced collapse of symbiotic nutrient cycling eventually leads to host starvation in cold-stressed Cnidaria. Hence, while cold and heat stress may invoke contrasting physiological effects on endosymbionts, our results suggest that both stressors destabilize the symbiosis through similar mechanisms rooted in host starvation. Plain language summary Ocean warming is the main cause of coral bleaching, but little is known about how cold affects the Cnidarian-algal symbiosis. Exposing the sea anemone Aiptasia couchii to cold stress, we observed reduced symbiont populations and disrupted carbon cycling, leading to lipid mobilization and protein breakdown. This suggests that, like heat stress, cold destabilizes the symbiosis through host starvation.