Most bacteria within aerated environments exist within a variety of dormant forms. In these states, bacteria adapt to adverse environmental conditions such as organic carbon starvation by reducing metabolic expenditure and potentially using alternative energy sources. In this study, we investigated the energy sources that could sustain persistence of the environmentally widespread bacterial phylum Chloroflexi. A transcriptome study revealed that Thermomicrobium roseum (class Chloroflexia) extensively remodels its respiratory chain after entering 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 highly expressed. We validated by gas chromatography and microsensor experiments that T. roseum oxidizes H2 and CO at a range of concentrations, including to sub-atmospheric levels, through an aerobic respiratory chain-dependent manner. Phylogenetic analyses suggests that the enzymes mediating these processes, namely group 1h [NiFe]-hydrogenases and type I carbon monoxide dehydrogenases, are widely distributed in Chloroflexi and were acquired on at least two separate occasions through horizontal gene transfer events. In support of this, we confirmed that the sporulating isolate Thermogemmatispora sp. T81 (class Ktedonobacteria) also scavenges H2 and CO during persistence. This study provides the first pure culture evidence that atmospheric carbon monoxide supports persistence of microorganisms. In addition, it reports the third phylum capable of mediating the biogeochemically and ecologically important process of atmospheric H2 oxidation. This adds to growing evidence that trace gases serve as dependable energy sources for dormant microorganisms.