Heterogeneous effects of heat and cold stress on carbon metabolism in coral-associated microorganisms

The high productivity of coral reef ecosystems depends on homeostatic regulation and efficient cycling of nutrients—particularly carbon—mediated by symbiotic organisms. Although both zooxanthellae and microbes are essential for coral carbon metabolism, their responses to temperature stress remain poorly understood. This study compared carbon metabolic profiles of thermally susceptible Acropora pruinosa and resilient Porites lutea under heat (30°C), ambient seawater (24°C), and cold (16°C) temperature conditions using integrated physiological and omics analyses. In A. pruinosa, heat stress reduced pigmentation, zooxanthellae density, and photosynthetic efficiency, with even stronger impairments under cold stress. Both temperature extremes, but especially cold stress, reshaped microbial composition, diversity, network complexity, and influenced carbon-related functional genes. In contrast, P. lutea exhibited partial inhibition of zooxanthellae and microbial carbon metabolism under both temperature extremes, reflecting greater resilience. The findings also indicate that zooxanthellae play a dominant role in sustaining carbon balance under temperature stress—especially cold—supporting a model in which zooxanthellae act as regulators and microbes as adaptors in maintaining carbon metabolic homeostasis. Overall, this study demonstrates species-specific sensitivity of corals to temperature stress as well as distinct, heterogeneous effects of low and high temperatures on carbon metabolism and sequestration efficiency of coral-associated microorganisms.