Abstract
Carbon monoxide (CO) is a ubiquitous atmospheric trace gas produced by natural and anthropogenic sources. Some aerobic bacteria can oxidize atmospheric CO and, collectively, they account for the net loss of ~250 teragrams of CO from the atmosphere each year. However, the physiological role, genetic basis, and ecological distribution of this process remain incompletely resolved. In this work, we addressed these knowledge gaps through culture-based and culture-independent work. We confirmed through shotgun proteomic and transcriptional analysis that the genetically tractable aerobic soil actinobacterium Mycobacterium smegmatis upregulates expression of a form I molydenum–copper carbon monoxide dehydrogenase by 50-fold when exhausted for organic carbon substrates. Whole-cell biochemical assays in wild-type and mutant backgrounds confirmed that this organism aerobically respires CO, including at sub-atmospheric concentrations, using the enzyme. Contrary to current paradigms on CO oxidation, the enzyme did not support chemolithoautotrophic growth and was dispensable for CO detoxification. However, it significantly enhanced long-term survival, suggesting that atmospheric CO serves a supplemental energy source during organic carbon starvation. Phylogenetic analysis indicated that atmospheric CO oxidation is widespread and an ancestral trait of CO dehydrogenases. Homologous enzymes are encoded by 685 sequenced species of bacteria and archaea, including from seven dominant soil phyla, and we confirmed genes encoding this enzyme are abundant and expressed in terrestrial and marine environments. On this basis, we propose a new survival-centric model for the evolution of aerobic CO oxidation and conclude that, like atmospheric H2, atmospheric CO is a major energy source supporting persistence of aerobic heterotrophic bacteria in deprived or changeable environments.
Highlights
Mycobacterium smegmatis mc2155 [66] and the derived strain ΔcoxL were maintained on lysogeny broth (LB) agar plates supplemented with 0.05% (w/v) Tween80
Levels of the two uptake hydrogenases increased, the catalytic subunit of hydrogenase-2 (HhyL, 148-fold), in line with previous observations that mycobacteria persist on atmospheric H2 [54, 63]
The proteome suggests that various energetically-expensive processes, such as cell wall, ribosome, and DNA synthesis, were downregulated (Table S2). These results suggest that M. smegmatis reduces its energy expenditure and expands its metabolic repertoire, including by oxidizing Carbon monoxide (CO), to stay energized during starvation
Summary
Through proteomic, genetic, and biochemical analyses, that its CO dehydrogenase is (i) strongly induced by organic carbon starvation, (ii) mediates aerobic respiration of atmospheric CO, and (iii) enhances survival of carbonstarved cells. On this basis, we confirm that atmospheric CO supports microbial survival and, with support from genomic, metagenomic, and metatranscriptomic analyses, propose a survival-centric model for the evolution and ecology of carboxydovores
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