Isolation and genomic and physiological characterization ofParageobacillussp. G301, the isolate capable of both hydrogenogenic and aerobic carbon monoxide oxidation

Abstract

Prokaryotes, known as carbon monoxide (CO) oxidizers, use CO as the carbon or energy source with CO dehydrogenases (CODHs), which are divided into nickel-containing CODH (Ni-CODH) that are sensitive to O2 and molybdenum-containing CODH (Mo-CODH) that are capable of aerobic functioning. The oxygen conditions for CO oxidizers to oxidize CO may be limited because CO oxidizers isolated and characterized so far have either Ni- or Mo-CODH. Here, we report a novel CO oxidizer capable of CO oxidation with both types of CODH based on genomic and physiological characterization of the isolate Parageobacillus sp. G301. This thermophilic facultative anaerobic Bacillota bacterium was isolated from the sediment of a freshwater lake. Genomic analyses showed that G301 was the only isolate possessing both Ni-CODH and Mo-CODH. Genome-based reconstruction of the respiratory machinery and physiological investigation indicated that CO oxidation by Ni-CODH was coupled with H2 production (proton reduction), and CO oxidation by Mo-CODH was coupled with O2 reduction under aerobic conditions and nitrate reduction under anaerobic conditions. G301 would thus be able to thrive via CO oxidation under a wide range of conditions, from aerobic environments to anaerobic environments even without terminal electron acceptors other than protons. As comparative genome analyses revealed no significant differences in genome structures and encoded cellular functions, except for CO oxidation between CO oxidizers and non-CO oxidizers in the genus Parageobacillus, CO oxidation genes would be retained exclusively for CO metabolism and related respiration. Importance Microbial CO oxidation has received a lot of attention because it contributes to global carbon cycling in addition to functioning as a remover of CO, which is toxic to many organisms. Microbial CO oxidizers have a punctate phylogenetic distribution throughout bacteria and archaea, even in genus-level monophyletic groups. In this study, we demonstrated that the new isolate Parageobacillus sp. G301 is capable of both anaerobic (hydrogenogenic) and aerobic CO oxidation, which had not been previously reported. The discovery of this new isolate, which is versatile in CO metabolism, would accelerate research into such CO oxidizers with diverse CO metabolisms, expanding our understanding of microbial diversity. Through comparative genomic analyses, we propose that CO oxidation genes are optional but not essential genetic elements in the genus Parageobacillus, providing insight into a factor that shapes the mosaic phylogenetic distribution of CO oxidizers, even in genus-level monophyletic groups.