Diversity and geographical distribution of potential carbon monoxide oxidizers using molybdenum-containing enzymes in...

Carbon monoxide (CO) evolves from photochemical or thermal reactions in the ocean. It is estimated that 90% of oceanic CO is consumed by CO-oxidizing prokaryotes, which convert CO to carbon dioxide using molybdenum-containing CO dehydrogenase (Mo-CODH). Investigation of form I cox, which encodes Mo-CODH, has revealed that oceanic prokaryotes with form I cox (potential cox-containing CO oxidizers: pcox-CO oxidizers) belong to eight phyla and occupy 10%-20% of prokaryotes. However, previous studies may have overestimated their diversity due to the use of less stringent criteria, and their ecology remains poorly understood. In this study, we characterized pcox-CO oxidizers by identifying form I cox from prokaryotic genomes reconstructed from the ocean. We used criteria that considered the phylogeny of Cox, their active site motifs, and the operon structure of cox. As a result, 233 species from nine phyla, which included 207 species unknown to be pcox-CO oxidizers, were found. We investigated the biogeography of each species and found 34 species that dominate in particular oceanic regions. Among the 34 species, 11 co-occurred with either of 20 prokaryotic species, and the co-occurring partners varied among species. No functional genes except those related to CO oxidation were shared between the 11 species, which implied the absence of common molecular basis that underlies ecological interaction between pcox-CO oxidizers and other prokaryotes. Finally, we performed absolute quantification of four species of pcox-CO oxidizers that were predicted to be dominant in Osaka Bay, Japan. It showed that pcox-CO oxidizers occupied over 8.49% of the bacterial community.IMPORTANCEThe ocean is a source of carbon monoxide (CO), an indirect greenhouse gas that supports the accumulation of methane and the production of a precursor of tropospheric ozone. The primary sink of CO in the ocean is prokaryotic CO oxidizers which possess molybdenum-containing CO dehydrogenase (Mo-CODH). Understanding CO flux therefore requires ecological characterization of prokaryotes carrying cox, which encode Mo-CODH. We provide a comprehensive, well-curated catalog of such prokaryotes (potential cox-containing CO oxidizers: pcox-CO oxidizers) in the ocean that not only revealed their diversity but also enabled species-specific ecological assessments. Co-occurrence analyses and genomic analysis of pcox-CO oxidizers uncovered substantial variation in their co-occurring prokaryotic partners and functional gene repertoires. The lack of shared co-occurrence and conserved genes suggests that CO oxidation via Mo-CODH does not mediate ecological interactions. These findings provide a foundation for future studies of pcox-CO oxidizers and offer new insight into ecological roles of CO oxidizers.