Phosphorus nutrition strategies in a Symbiodiniacean species: Implications in coral-alga symbiosis facing increasing phosphorus deficiency in future warmer oceans

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, our understanding on how symbiotic algae cope with P deficiency is limited. Here, we investigated the responses of a coral symbiotic species of Symbiodiniaceae, Cladocopium goreaui, to P-limitation by examining its physiological performance and transcriptomic profile. Under P stress, C. goreaui exhibited decreases in algal growth, photosynthetic efficiency, and cellular P content but enhancement in carbon fixation, N assimilation, N:P ratio, and energy metabolism, with downregulated expression of carbohydrate exporter genes. Besides, C. goreaui showed flexible mechanisms of utilizing different dissolved organic phosphorus to relieve P deficiency. When provided glycerol phosphate, C. goreaui hydrolyzed it extracellularly to produce phosphate for uptake. When grown on phytate, in contrast, C. goreaui upregulated the endocytosis pathway while no dissolved inorganic phosphorus was released into the medium, suggesting that phytate was transported into the cell, potentially via the endocytosis pathway. This study sheds light on the survival strategies of C. goreaui and potential weakening of its role as an organic carbon supplier in P-limited environments, underscoring the importance of more systematic investigation on future projections of such effects. 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 in coral reefs. We found that a coral symbiotic species of Symbiodiniaceae, Cladocopium goreaui, exhibited decreased photosynthetic efficiency and downregulated carbohydrate exporter genes but enhanced carbon fixation, N assimilation, and energy metabolism under P limitation and showed flexible mechanisms of dissolved organic phosphorus utilization to relieve P deficiency. This study sheds light on the survival strategies of symbiotic algae and potential weakening of its role as an organic carbon supplier under P limitation.image