Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide

Abstract Bacteria within aerated environments often exist within a variety of dormant forms. In these states, bacteria endure adverse environmental conditions such as organic carbon starvation by decreasing metabolic expenditure and using alternative energy sources. In this study, we investigated the energy sources that facilitate the persistence of the environmentally widespread but understudied bacterial phylum Chloroflexi. A transcriptome study revealed that Thermomicrobium roseum (class Chloroflexia) extensively remodels its respiratory chain upon entry into stationary phase due to organic carbon limitation. Whereas primary dehydrogenases associated with heterotrophic respiration were downregulated, putative operons encoding enzymes involved in molecular hydrogen (H2), carbon monoxide (CO), and sulfur compound oxidation were significantly upregulated. Gas chromatography and microsensor experiments were used to show that T. roseum aerobically respires H2 and CO at a range of environmentally relevant concentrations to sub-atmospheric levels. Phylogenetic analysis suggests that the enzymes mediating atmospheric H2 and CO oxidation, namely group 1h [NiFe]-hydrogenases and type I carbon monoxide dehydrogenases, are widely distributed in Chloroflexi genomes and have been acquired on at least two occasions through separate horizontal gene transfer events. Consistently, we confirmed that the sporulating isolate Thermogemmatispora sp. T81 (class Ktedonobacteria) also oxidises atmospheric H2 and CO during persistence. This study provides the first axenic culture evidence that atmospheric CO supports bacterial persistence and reports the third phylum to be experimentally shown to mediate the biogeochemically and ecologically important process of atmospheric H2 oxidation. This adds to the growing body of evidence that atmospheric trace gases serve as dependable energy sources for the survival of dormant microorganisms.