Distinction in Symbiodiniaceae and Bacterial Communities and Symbiodiniaceae Lineage-Specific Transcriptome...

Fine-scale thermal heterogeneity within intertidal and subtidal microhabitats could drive divergence in organismal heat tolerance. Reef corals from the extreme intertidal may hold optimism for the future of coral reefs and give insights into the mechanisms by which coral may persist under future conditions. Here, we compared the thermal sensitivities of intertidal and subtidal Acropora digitifera and evaluated their bleaching phenotypes, transcriptomes, host genetic differentiation and bacterial communities. Results showed that only heat-exposed subtidal corals displayed significantly reduced photochemical efficiency, symbiont densities, pigment and host protein concentrations, suggesting bleaching and host starvation. Despite being genetically similar, heat-exposed subtidal corals mounted stronger immune activation and amino acid degradation but downregulated monocarboxylate transport and calcification compared to intertidal corals. In contrast to the prevalence of Cladocopium in subtidal corals, intertidal corals were dominated by Durusdinium, whose transcriptional signature was characterised by lineage-specific and constitutively high transcript abundance of orthologs involved in stress response, metabolism, photosynthesis, cell cycle and symbiotic interactions. Furthermore, 16S rRNA sequencing demonstrated an origin-dependent bacterial composition, with Endozoicomonas being more abundant and important in co-occurrence networks of intertidal corals. Our findings suggest that distinction in Symbiodiniaceae and bacterial communities and Symbiodiniaceae lineage-specific transcriptional footprint largely underpin the exceptional thermotolerance of intertidal Acropora. Although these corals provide promising avenues for restoration, such a mechanism may bring attention to the risk of using them in selective breeding, particularly given the horizontal transmission of algal symbionts in Acropora.