Coral reefs are increasingly threatened by global climate change, and mass bleaching and mortality events caused by elevated seawater temperature have led to coral loss worldwide. Hainan Island hosts extensive coral reef ecosystems in China, yet seasonal variation in Symbiodiniaceae communities within this region remains insufficiently understood. We aimed to investigate the temperature-driven adaptability regulation of the symbiotic Symbiodiniaceae community in reef-building corals, focusing on the environmental adaptive changes in its community structure in coral reefs between cold (23.6–24.6 °C) and warm (28.2–30.6 °C) months. Symbiodiniaceae shuffling and rare genotype turnover were discovered in adaptability variations in the symbiotic Symbiodiniaceae community between two months. Symbiodiniaceae genetic diversity increased during warm months, primarily due to temporal turnover of rare genotypes within the Cladocopium and Durusdinium genera. Coral Favites, Galaxea, and Porites exhibited the shuffling of Symbiodiniaceae between tolerant Durusdinium and sensitive Cladocopium. Symbiodiniaceae interactions in G. fascicularis and P. lutea exhibited the highest levels of stability with the increase in temperature, whereas the interactions in A. digitifera and P. damicornis showed the lowest levels of stability. Rare genotypes functioned as central hubs and important roles within Symbiodiniaceae communities, exhibiting minimal responsiveness to temperature fluctuations while maintaining community structural stability. The temperature-driven adaptability regulation of symbiotic Symbiodiniaceae could be achieved by Symbiodiniaceae shuffling and rare genotype turnover. The process might be aggravated by concurrent adverse factors, including elevated salinity, pollution, and anthropogenic disturbance. These findings provide insights into how the Symbiodiniaceae community influences the adaptation and resilience of coral hosts to temperature fluctuations in coral reefs. Furthermore, they may contribute to assessing the reef-building coral’s capacity to withstand environmental stressors associated with global climate change.

Ocean acidification (OA), driven by global climate change together with pollution from organic contaminants, is increasing the ecological risk faced by coral reef ecosystems. The coral holobiont comprises diverse microbial communities that collectively support the coral host in coping with and adapting to environmental stress. However, the response of the coral holobiont to the combined stress of acidification and benzo[a]pyrene (BaP) remains poorly understood. In this study, Acropora millepora was selected as a model species to investigate the responses of coral-associated microbiomes to acidification (pH 7.8), BaP exposure (10 µg·L⁻¹) and their combined effects. We found that while the cell density of coral-associated Symbiodiniaceae increased significantly with prolonged exposure time in all treatment groups, and there were no temporal differences in chlorophyll-a contents. The Symbiodiniaceae community was stable within all treatments, with Cladocopium as the dominant genus, and subtype C3u had the highest relative abundance (>70%). A rapid and significant increase in rare bacteria taxa was observed in the single-stress treatments (acidification, BaP), whereas prolonged exposure led to an increasing number of unique bacteria taxa in the combined-stress group in two weeks. Surprisingly, the main community structure of core coral-associated bacteria in the combined treatment group was close to that of the control group. Across all treatments, core coral-associated bacteria (including Sphingomonadaceae and Burkholderiaceae) consistently dominated the microbial community, while core coral-associated archaea exhibited more stochastic variations. Collectively, these results highlight the critical role of coral-associated microbiomes in rapidly and flexibly responding to environmental stressors, thereby contributing to the maintenance of holobiont stability under multiple stress conditions.