Antioxidant capacity is a key factor in the difference in thermal tolerance between massive Porites lutea and branching Acropora formosa.

Identifying the reasons behind differences in thermal tolerance among reef-building corals is pivotal to projecting their ability to withstand increasing seawater temperatures. Antioxidant responses are common in marine organisms and are strongly linked with coral thermotolerance. However, the mechanism by which the antioxidant response affects the thermotolerance of coral holobionts remains unclear. In this study, heat stress experiments were performed on massive Porites lutea and branching Acropora formosa from Weizhou Island in the northern South China Sea and analyzed for physiological indices, antioxidant levels, and high-throughput sequencing. Following heat stress, A. formosa exhibited more severe physiological bleaching and significantly lower Symbiodiniaceae density, Fv/Fm, and antioxidant levels than P. lutea. Moreover, P. lutea host and its Symbiodiniaceae (Cladocopium C15) downregulated fewer antioxidant-related genes than A. formosa at 34 °C. Specifically, P. lutea host had a more complex antioxidant regulatory capacity and mainly regulated glutathione (GSH). Cladocopium C15 enhanced the regulation of GSH, peroxisome, and ascorbate-related genes, thereby boosting antioxidant capacity. P. lutea also had more antioxidant-functional coral-associated bacteria than A. formosa at high temperatures, including Endozoicomonas, Ruegeria, and Dinoroseobacter. Overall, the superior antioxidant capacity of the coral holobionts plays a key role in the greater thermotolerance of P. lutea. These findings suggest that antioxidants can potentially be used as biomarkers for coral reef management. Our research deepens the understanding of high-temperature adaptation strategies for thermotolerant corals and provides a theoretical basis for their selection and reef restoration.