19Carbon monoxide (CO) is a ubiquitous atmospheric trace gas produced by natural and 20 anthropogenic sources. Some aerobic bacteria can oxidize atmospheric CO and, 21 collectively, they account for the net loss of ~250 teragrams of CO from the 22 atmosphere each year. However, the physiological role, genetic basis, and ecological 23 distribution of this process remain incompletely resolved. In this work, we addressed 24 these knowledge gaps through culture-based and culture-independent work. We 25 confirmed through shotgun proteomic and transcriptional analysis that the genetically 26 tractable aerobic soil actinobacterium Mycobacterium smegmatis upregulates 27 expression of a carbon monoxide dehydrogenase by 50-fold when exhausted for 28 organic carbon substrates. Whole-cell biochemical assays in wild-type and mutant 29 backgrounds confirmed that this organism aerobically respires CO, including at sub-30 atmospheric concentrations, using the enzyme. Contrary to current paradigms on CO 31 oxidation, the enzyme did not support chemolithoautotrophic growth and was 32 dispensable for CO detoxification. However, it significantly enhanced long-term 33 survival, suggesting that atmospheric CO serves a supplemental energy source during 34 organic carbon starvation. Phylogenetic analysis indicated that atmospheric CO 35 oxidation is widespread and an ancestral trait of CO dehydrogenases. Homologous 36 enzymes are encoded by 685 sequenced species of bacteria and archaea, including 37 from seven dominant soil phyla, and we confirmed genes encoding this enzyme are 38 abundant and expressed in terrestrial and marine environments. On this basis, we 39 propose a new survival-centric model for the evolution of CO oxidation and conclude 40 that, like atmospheric H2, atmospheric CO is a major energy source supporting 41 persistence of aerobic heterotrophic bacteria in deprived or changeable environments.42 43 45 natural processes and anthropogenic pollution. The average global mixing ratio of this 46 gas is approximately 90 ppbv in the troposphere (lower atmosphere), though this 47 concentration greatly varies across time and space, with levels particularly high in 48 urban areas [1-4]. Currently, human activity is responsible for approximately 60% of 49 emissions, with the remainder attributable to natural processes [1]. Counteracting 50these emissions, CO is rapidly removed from the atmosphere (lifetime of two months) 51 by two major processes: geochemical oxidation by atmospheric hydroxyl radicals 52 (85%) and biological oxidation by soil microorganisms (10%) [1, 5]. Soil 53 microorganisms account for the net consumption of approximately 250 teragrams of 54 atmospheric CO [1, 5, 6]; on a molar basis, this amount is seven times higher than the 55 amount of methane consumed by soil bacteria [7]. Aerobic CO-oxidizing 56 microorganisms are also abundant in the oceans; while oceans are a minor source of 57 atmospheric CO overall [8,9], this reflects that substantial amounts of the gas are 58 produced photochemically within...