Phosphate deficiency promotes coral bleaching and is reflected by the ultrastructure of symbiotic dinoflagellates

Enrichment of reef environments with dissolved inorganic nutrients is considered a major threat to the survival of corals living in symbiosis with dinoflagellates (Symbiodinium sp.). We argue, however, that the direct negative effects on the symbiosis are not necessarily caused by the nutrient enrichment itself but by the phosphorus starvation of the algal symbionts that can be caused by skewed nitrogen (N) to phosphorus (P) ratios. We exposed corals to imbalanced N:P ratios in long-term experiments and found that the undersupply of phosphate severely disturbed the symbiosis, indicated by the loss of coral biomass, malfunctioning of algal photosynthesis and bleaching of the corals. In contrast, the corals tolerated an undersupply with nitrogen at high phosphate concentrations without negative effects on symbiont photosynthesis, suggesting a better adaptation to nitrogen limitation. Transmission electron microscopy analysis revealed that the signatures of ultrastructural biomarkers represent versatile tools for the classification of nutrient stress in symbiotic algae. Notably, high N:P ratios in the water were clearly identified by the accumulation of uric acid crystals. •Undersupply with dissolved inorganic phosphate causes coral bleaching.•Ultrastructural biomarkers in algal symbionts identify nutrient stress in reef corals.•Uric acid crystals in zooxanthellae identify high N:P ratios in the water column.•Nitrate enrichment of the water causes phosphate deficiency in Symbiodinium.•Coral symbionts tolerate nitrogen limitation better than phosphorus limitation.