Undocumented potential for primary productivity in a globally-distributed bacterial photoautotroph

Aerobic anoxygenic phototrophs (AAnPs) are common in the global oceans and are associated with photoheterotrophic activity. To date, AAnPs have not been identified in the surface ocean that possess the potential for carbon fixation. Using the Tara Oceans metagenomic dataset, we have reconstructed draft genomes of four bacteria that possess the genomic potential for anoxygenic phototrophy, carbon fixation via the Calvin-Benson-Bassham cycle, and the oxidation of sulfite and thiosulfate. Forming a monophyletic clade within the Alphaproteobacteria and lacking cultured representatives, the organisms compose minor constituents of local microbial communities (0.1-1.0%), but are globally distributed, present in multiple samples from the North Pacific, Mediterranean Sea, the East Africa Coastal Province, and the South Atlantic. These organisms represent a shift in our understanding of microbially-mediated photoautotrophy in the global oceans and provide a previously undiscovered route of primary productivity.Significance StatementIn examining the genomic content of organisms collected during the Tara Oceans expedition, we have identified a novel clade within the Alphaproteobacteria that has the potential for photoautotrophy. Based on genome observations, these organisms have the potential to couple inorganic sulfur compounds as electron donors to fix carbon into biomass. They are globally distributed, present in samples from the North Pacific, Mediterranean Sea, East Africa Coastal Current, and the South Atlantic. This discovery may require re-examination of the microbial communities in the global ocean to understand and constrain the impacts of this group of organisms on the global carbon cycle.