The role of holobiont composition and environmental history in thermotolerance of Tropical Eastern Pacific corals

Coral reefs support approximately 25% of all marine life, making it essential to understand the factors impacting their ability to withstand climate change. Corals’ response mechanisms encompass both the host's own potential and that of a diverse microbial community, collectively known as the holobiont. Research investigating how these co-evolved taxa affect each other during thermal stress has revealed both the vulnerability and resilience of coral reefs, but the precise mechanisms underlying different bleaching trajectories are still poorly understood. We implemented a standardized acute thermal stress assay to investigate how seasonal upwelling in Panama's Tropical Eastern Pacific (TEP) influences Pocillopora coral's host-microbiome configurations, and we tested holobionts’ resistance to increasing temperatures. Despite little host genetic differentiation, algal community shifts were modulated by both region and genetic lineage. This pattern strongly contrasted with temperature-driven dysbiosis for the prokaryotic community. Host stress responses differed among regions during acute thermal stress. Regional variation in total antioxidant capacity suggested that corals from the region with seasonal upwelling experience more stressful baseline conditions, which may contribute to their higher predicted thermal thresholds as estimated via host protein concentrations. Furthermore, shifts in algal microbiomes were associated with changes in host thermotolerance, as captured by host physiology and oxidative metabolism, suggesting a possible link between microbiome composition and host physiological performance. By leveraging the natural laboratory created by Panama's TEP, we demonstrate that coral holobionts from nearby gulfs with different thermal dynamics differ in their ability to withstand thermal stress, providing new insights into the factors driving coral thermotolerance.