RNAseq samples distribution.

Climate change driven ocean warming is causing widespread degradation of coral reefs. In the Florida Keys, many reefs have lost much of their coral cover, yet some inshore reefs have maintained higher coral cover and exhibited higher bleaching resistance and resilience than reefs offshore during marine heatwave events. To explore the molecular mechanisms underlying the higher heat tolerance observed on inshore reefs, we subjected three inshore and four offshore genotypes of the coral Orbicella faveolata to 30, 31, 32, or 33°C for 31 days and measured photochemical efficiency (Fv/Fm), the species and relative abundance of dinoflagellate endosymbionts, and gene expression of the host and symbiont. All inshore coral genotypes, regardless of symbiont species, were significantly more thermotolerant than offshore genotypes based on comparatively smaller declines in photochemical efficiently. The most heat-tolerant inshore genotype (In1) was dominated by the symbiont Durusdinium trenchii; all other genotypes, both inshore and offshore, were Breviolum minutum-dominated, suggesting local adaptation or acclimatization contributes to the heat tolerance of inshore genotypes not dominated by D. trenchii. After 31 days of heat stress, all coral genotypes (except In2) had lost most of their B. minutum and became dominated by D. trenchii. Host genotype In1 presented unique expression patterns of genes involved in heat shock response, immunity, and protein degradation. There were fewer changes in the symbiont gene expression of inshore corals under heat stress when compared to the offshore colonies, which experienced significant changes, including increases in ribosomal and photosynthetic proteins. These data show that the differential thermotolerance between inshore and offshore O. faveolata in the Florida Keys is associated with statistically significant differences in both host and symbiont gene expression that provide insights into the mechanisms underlying holobiont heat tolerance.由气候变化引发的海洋变暖正造成珊瑚礁的广泛退化。在佛罗里达礁岛群，多数珊瑚礁已大幅丧失珊瑚覆盖度，但部分近岸珊瑚礁在海洋热浪事件中，仍维持了更高的珊瑚覆盖度，且展现出比离岸珊瑚礁更强的抗漂白能力与恢复力。为探究近岸珊瑚礁所观测到的更高耐热性背后的分子机制，我们将珊瑚Orbicella faveolata的3个近岸基因型与4个离岸基因型分别暴露于30、31、32或33℃的环境中培养31天，并测定了光化学效率（Fv/Fm）、甲藻内共生体的物种组成与相对丰度，以及宿主与共生体的基因表达情况。无论共生体物种为何，所有近岸珊瑚基因型的耐热性均显著高于离岸基因型，这一点通过其光化学效率的下降幅度相对更小得以体现。耐热性最强的近岸基因型（In1）以共生体Durusdinium trenchii为优势类群；其余所有近岸与离岸基因型均以Breviolum minutum为优势类群，这表明除了以D. trenchii为优势类群的近岸基因型外，本地适应或驯化也有助于提升近岸基因型的耐热性。经过31天的热胁迫后，除In2外的所有珊瑚基因型均已丧失大部分B. minutum，并转而以D. trenchii为优势类群。宿主基因型In1展现出参与热休克响应、免疫反应与蛋白质降解过程的基因的独特表达模式。与经历了显著基因表达变化的离岸珊瑚群落相比，近岸珊瑚的共生体基因表达在热胁迫下的变化幅度更小，这些变化包括核糖体蛋白与光合蛋白编码基因的表达上调。这些数据表明，佛罗里达礁岛群近岸与离岸Orbicella faveolata之间的耐热性差异，与宿主和共生体基因表达的统计学显著差异相关，这些差异为阐明共生功能体（holobiont）耐热性的潜在机制提供了见解。