Diversity, abundance, and expression of proteorhodopsin genes in the northern South China Sea

Proteorhodopsins have been suggested as an important strategy among phototrophs to capture solar energy in marine environments. The goals of this study was to investigate the diversity of proteorhodopsin genes and to explore their abundance, distribution, and expression in the coastal surface waters of the northern South China Sea, one of the largest marginal seas of the western North Pacific Ocean. Using 21 metagenomes, we recovered proteorhodopsin genes from a wide range of prokaryotic taxa, and chlorophyll a contributed significantly to the community composition of proteorhodopsin-containing microbes. Most proteorhodopsin sequences were predicted to encode green light-absorbing proton pumps and green light-absorbing proteorhodopsin genes were more abundant than blue-absorbing ones. The variations in the conserved residues involved in ion pumping and several uncharacterized proteorhodopsins were observed. The gene abundance pattern of proteorhodopsin types were significantly influenced by the levels of total organic carbon and soluble reactive phosphorus. Gene expression analysis confirmed the importance of proteorhodopsin-based phototrophy and revealed different expressional patterns among major phyla. In tandem, we screened 2295 metagenome-assembled genomes to describe the taxonomic distribution of proteorhodopsins. Bacteroidota are the key lineages encoding proteorhodopsins, but proteorhodopsins were predicated from members of Proteobacteria, Marinisomatota, Myxococcota, Verrucomicrobiota and Thermoplasmatota. Our study expanded the diversity of proteorhodopsins and improve our understanding on the significance of proteorhodopsin-mediated phototrophy in the marine ecosystem. •Proteorhodopsin genes are abundant and originated from a wide range of prokaryotic taxa in the northern South China Sea.•Chlorophyll a was a significant contributor in shaping the community composition of proteorhodopsin-containing microbes.•Proteorhodopsin-containing microbes exploit various light spectrums and have potentially novel proteorhodopsin functions.•Total organic carbon and soluble reactive phosphorus were the key environmental drivers for proteorhodopsin types.•The abundant Bacteroidota had blue light-absorbing proteorhodopsin and genomes with multiple proteorhodopsin gene copies.