Reef-scale environmental mosaics shape coral physiological and microbial signatures of resilience

Abstract

Environmental variability shapes coral performance, yet its role in structuring host physiology and microbiome composition across reef habitats remains unresolved. We investigated six geomorphologically distinct sites across Heron Island, southern Great Barrier Reef, as a natural laboratory to test how life-long exposure to distinct environmental regimes influences the holobiont of the coral Pocillopora damicornis. We paired one year of high-frequency physiochemical records (including temperature, dissolved oxygen, light, salinity, chlorophyll fluorescence, and turbidity) with measurements of coral physiology, Symbiodiniaceae profiles, and bacterial community composition. Sites differed in their overall environmental regimes, including a nearly threefold range in mean diel temperature variability (1.12–3.39°C day-1), which emerged as the primary driver of physiological differences. Host and symbiont genotyping confirmed all corals matched P. damicornis and Symbiodiniaceae communities were dominated by Cladocopium latusorum. Corals from the intermediately variable site exhibited the highest tissue biomass, chlorophyll-a, and mycosporine-like amino acid content, aligning with the greatest thermal tolerance and resulting in a physiologically distinct phenotype. Colonies from the most variable sites demonstrated higher thermal tolerance than the stable sites, but exhibited energy allocation away from biomass accumulation and reserve storage. Despite a conserved Endozoicomonadaceae-dominated core microbiome, site-specific variation in families such as Cyanobiaceae, Pseudoalteromonadaceae, Microtrichaceae, and Moraxellaceae suggests that environmentally responsive microbes may contribute disproportionately to holobiont physiology across reef habitats. Together, these findings show that reef-scale environmental mosaics generate distinct holobiont phenotypes and suggest that intermediate, rather than extreme, environmental variability may best support coral physiological condition, rather than maximizing performance across all ecological functions.