Metabolic dynamics of the coral-algal symbiosis from fertilization to settlement identify critical coral energetic vulnerabilities

Climate change accelerates coral reef decline and jeopardizes recruitment essential for ecosystem recovery. Adult corals rely on a vital nutritional exchange with their symbiotic algae (Symbiodiniaceae), but the dynamics and sensitivity of this reliance from fertilization to recruitment are understudied. We investigated the physiological, metabolomic, and transcriptomic changes across 13 developmental stages of Montipora capitata, a coral in Hawai i that inherits symbionts from parent to egg. We found that embryonic development depends on maternally provisioned mRNAs and lipids, with a rapid shift to symbiont-derived nutrition in swimming larvae. Symbiont density and photosynthesis peak once swimming to fuel pelagic larval dispersal. In contrast, respiratory demand increases significantly during metamorphosis, settlement, and calcification, reflecting this energy-intensive morphological reorganization. Symbiont ontogenetic proliferation is driven by symbiont ammonium assimilation with little evidence of nitrogen metabolism in the coral host. As development progresses, the host enhances nitrogen sequestration, regulating symbiont populations, and ensuring the transfer of fixed carbon to support metamorphosis, with both metabolomic and transcriptomic indicators of increased carbohydrate availability. Although algal symbiont communities remained stable, bacterial communities shifted with ontogeny, associated with holobiont metabolic reorganization. Our study reveals extensive metabolic changes during development, increasingly reliant on symbiont nutrition. Metamorphosis and settlement emerge as the most critical periods of energetic vulnerability to projected climate scenarios that destabilize symbiosis. This highly detailed elucidation of symbiotic nutritional exchange relative to sensitive early life stages provides essential knowledge for understanding and forecasting nutritional symbiosis integration, and specifically, coral survival and recruitment in a future of climate change.