Coral reefs thrive in the oligotrophic ocean and rely on symbiotic algae to acquire nutrients. Global warming is projected to intensify surface ocean nutrient deficiency and anthropogenic discharge of wastes with high nitrogen (N): phosphorus (P) ratios can exacerbate P nutrient limitation. However, how coral‐alga symbiosis copes with stoichiometric P deficiency and thermal stress to regulate coral-Symbiodiniaceae mutualism is limited. Here, we investigated the adaption strategies of a wide-distributed Symbiodiniaceae Cladocopium goreaui and a coral-derived Symbiodinium strain, to P-limitation and heat stress by examining its physiological performance and transcriptomic profile. Under P stress, C. goreaui exhibited decreases in cellular P content but enhancement in carbon fixation, N assimilation, N:P ratio, and energy metabolism, with downregulated expression of carbohydrate exporter genes. More important, C. goreaui employed flexible mechanisms of utilizing different dissolved organic phosphorus to relieve P deficiency. Nevertheless, the heat and P-limitation co-stress repressed the expression of N uptake and assimilation genes in Symbiodinium. Moreover, P limitation intensified downregulation of carbon fixation (light and dark reaction) and metabolism (glycolysis) pathways in heat-stressed Symbiodinium. Notably, co-stress elicited a marked transcriptional downregulation of genes encoding photosynthates transporters and microbe-associated molecular patterns, potentially undermining the mutualism potential. Our results indicate that nutrient imbalance in the coral reef ecosystem can intensify heat-stress effects on the mutualistic capacity of Symbiodiniaceae. This work sheds light on the survival strategies of symbionts and potential weakening of their role as an organic carbon supplier in coral-algae holobionts in the warming and increasingly nutrient-imbalanced ocean, underscoring the importance of more systematic investigation on future projections of such effects.

phosphorus limitation,heat stress,Symbiodiniaceae,symbiosis,adaption mechanism