Proton-pumping rhodopsin of the coral symbiont Breviolum minutum and its potential role in coping with phosphorus deficiency in future warmer ocean

Global warming can inhibit chlorophyll-based solar energy capturing of phytoplankton by decreasing nutrient supply through upwelling. However, species with proton-pump rhodopsin (PPR) can independently convert solar energy to cope with nutrient limitation. Besides prokaryotes, PPR has been documented in dinoflagellates and some species of other algal lineages, and its potential role in compensating for the deficiency of phosphorus has been demonstrated in dinoflagellates. However, PPR has not been studied in the coral reef endosymbiotic Symbiodiniaceae. Here, we report a PPR in Breviolum minutum (BmR). Both phylogenetic analysis and structure prediction results indicate that BmR resembles eukaryotic proton-pump rhodopsins, phylogenetically affiliated with the subgroup xanthorhodopsins. BmR contains the critical residues for proton pumping, retinal binding, and spectrum tuning for green absorption. To explore BmR’s potential roles in responding to phosphorus limitation, we cultured B. minutum under different phosphorus conditions, and monitored physiological and BmR’s transcriptional responses. Phosphorus limitation caused decreases in B. minutum population growth and photosynthesis efficiency. Meanwhile, our quantitative PCR showed that BmR expression was strongly upregulated under phosphorus limitation, showing a strong positive correlation with alkaline phosphatase activity and a negative correlation with photosynthetic efficiency. Our findings demonstrate that proton-pump rhodopsin occurs in Symbiodiniaceae and BmR has the potential to provide supplementary energy to support cell basal metabolisms when photosynthesis of B. minutum is impaired by phosphorus limitation, thereby enabling corals to better weather climate change.