Seasonal Variation in In Hospite but Not Free-Living, Symbiodiniaceae Communities Around Hainan Island, China

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.