Nutritional exchange between reef-building corals and algal endosymbionts buffers the energetic demand of larval development and metamorphosis

Anthropogenic climate change threatens the persistence of coral reefs by impacting reproduction and accelerating coral loss. Adult corals depend on nutritional exchange with their endosymbiotic algae (Symbiodiniaceae) to fulfill their energetic demands. However, the mechanisms underlying the onset of this exchange during early life stages and how it contributes to developmental energy demands are unclear. We conducted an integrative analysis of metabolism across developmental stages in Montipora capitata, a vertically transmitting coral (Symbiodiniaceae are passed from parent to offspring) in Hawai□i. We applied physiological (metabolism and symbiont density) and multi-omic (metabolomics, transcriptomics, and microbial amplicon sequencing) approaches over 13 time points between 1-255 hours post-fertilization from eggs to settled recruits. Energetic demand (respiration) increased as embryos developed into larvae and progressed through metamorphosis. Symbiont photosynthetic capacity (photosynthesis and cell density) increased across ontogeny, demonstrating potential for symbiont-derived nutrition to fuel coral development and growth. Indeed, gene expression and metabolomic analyses revealed that symbiont-derived nutrition is metabolized starting in the motile larval stage with increasing utilization during metamorphosis and following settlement. Specifically, gene and metabolic pathways associated with organic compound transport and glucose and fatty acid metabolism were enriched and there was expanded use of carbohydrate and lipid metabolism in metamorphosed polyps and recruits. Larvae also demonstrate increased cellular processes to maintain nutrient balance between host and symbiont and regulate symbiont populations through expression of genes that regulate nitrogen assimilation and response to reactive oxygen species. Collectively, our multi-omic characterization reveals that symbiont-derived nutrition becomes increasingly important to buffer energetic demands required for coral settlement. In environmentally stressful conditions, early life stages of vertically transmitting species may be increasingly vulnerable to the loss of symbiont-derived nutrition. Therefore, early interventions to reduce symbiotic stress during sensitive developmental stages could enhance coral reef recruitment and recovery as climate change intensifies.