Maintenance cost of photosynthesis sets key ecological constraints on zooxanthellate corals

Abstract

Ecological models using light limitation to explain coral depth distribution have largely disregarded the energetic cost of sustaining photosynthetic activity. Here, we quantified photosystem II (PSII) turnover across a depth-simulated light gradient in a zooxanthellate coral, measuring PSII half-life, D1 protein abundance, and PSII-complex gene expression. Maximum photosynthetic capacity remained stable across irradiance levels while respiration rose and PSII turnover accelerated as a power law, imposing increasing ATP demand at the shallowest depths. Declining D1 protein abundance alongside stable transcript levels demonstrated that this escalating maintenance cost operates through post-transcriptional regulation. Consequently, a decreasing fraction of photosynthetic usable energy is available for translocation to the coral host at high irradiance, as the energy required for PSII repair increases. Integrating these physiological constraints into a bio-optical model revealed that the balance between photosynthetic capacity and its maintenance cost defines an optimal depth, the Photosynthetic Usable Energy Supply (PUES) maximum, where host energetic returns are maximized. This framework provides a mechanistic basis for understanding depth distributions in symbiotic corals and extends as a predictive tool for any photosynthetic organism operating under variable irradiance, including forecasting how environmental degradation contracts viable depth ranges.