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Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis

Significance Coral growth and calcification is supported by sugars acquired from symbiotic algae, allowing corals to thrive in otherwise nutrient-poor environments. This symbiosis depends on the coordinated exchange of compounds between partners, the mechanisms of which are poorly understood. Here we found that coral host cells acidify the microenvironment where the symbiotic algae reside using a proton pump, the V-type H+-ATPase (VHA), which is present in the host membrane surrounding the algae. Acidification of the algal microenvironment by VHA promotes photosynthesis, demonstrating that the coral host can actively regulate symbiont physiology. This work is an important step toward understanding how animal symbioses function and provides mechanistic models that can help understand the capacity of corals to adapt to global climate change. Symbiotic dinoflagellate algae residing inside coral tissues supply the host with the majority of their energy requirements through the translocation of photosynthetically fixed carbon. The algae, in turn, rely on the host for the supply of inorganic carbon. Carbon must be concentrated as CO2 in order for photosynthesis to proceed, and here we show that the coral host plays an active role in this process. The host-derived symbiosome membrane surrounding the algae abundantly expresses vacuolar H+-ATPase (VHA), which acidifies the symbiosome space down to pH ∼4. Inhibition of VHA results in a significant decrease in average H+ activity in the symbiosome of up to 75% and a significant reduction in O2 production rate, a measure of photosynthetic activity. These results suggest that host VHA is part of a previously unidentified carbon concentrating mechanism for algal photosynthesis and provide mechanistic evidence that coral host cells can actively modulate the physiology of their symbionts.