Abstract
Microbial adaptation to extreme conditions takes many forms, including specialized metabolism which may be crucial to survival in adverse conditions. Here, we analyze the diversity and environmental importance of systems allowing microbial carbon monoxide (CO) metabolism. CO is a toxic gas that can poison most organisms because of its tight binding to metalloproteins. Microbial CO uptake was first noted by Kluyver and Schnellen in 1947, and since then many microbes using CO via oxidation have emerged. Many strains use molecular oxygen as the electron acceptor for aerobic oxidation of CO using Mo-containing CO oxidoreductase enzymes named CO dehydrogenase. Anaerobic carboxydotrophs oxidize CO using CooS enzymes that contain Ni/Fe catalytic centers and are unrelated to CO dehydrogenase. Though rare on Earth in free form, CO is an important intermediate compound in anaerobic carbon cycling, as it can be coupled to acetogenesis, methanogenesis, hydrogenogenesis, and metal reduction. Many microbial species—both bacteria and archaea—have been shown to use CO to conserve energy or fix cell carbon or both. Microbial CO formation is also very common. Carboxydotrophs thus glean energy and fix carbon from a “metabolic leftover” that is not consumed by, and is toxic to, most microorganisms. Surprisingly, many species are able to thrive under culture headspaces sometimes exceeding 1 atmosphere of CO. It appears that carboxydotrophs are adapted to provide a metabolic “currency exchange” system in microbial communities in which CO arising either abiotically or biogenically is converted to CO 2 and H 2 that feed major metabolic pathways for energy conservation or carbon fixation. Solventogenic CO metabolism has been exploited to construct very large gas fermentation plants converting CO-rich industrial flue emissions into biofuels and chemical feedstocks, creating renewable energy while mitigating global warming. The use of thermostable CO dehydrogenase enzymes to construct sensitive CO gas sensors is also in progress.
Highlights
Public perception of the role of carbon monoxide (CO) in biology is dominated by its reputation as a silent killer because of its toxicity
The Wood–Ljungdahl (WL) pathway depicted in Figure 1B is a highly adaptable set of enzymes that allow acetate formation by acetogens as well as anaplerotic feeding through the production of acetyl-CoA in many autotrophic bacteria and archaea
Diversification of the pathway during evolution allowed CO oxidation to be coupled to various metabolic processes ranging from energy conservation to carbon acquisition, metal reduction/ detoxification, and coping with oxidative stress
Summary
Public perception of the role of carbon monoxide (CO) in biology is dominated by its reputation as a silent killer because of its toxicity. C. hydrogenoformans has the ability to regulate the distribution of CO into different pathways by gene regulation through two different CO-binding CooA proteins that bind CO and induce CO gene clusters differentially at different CO concentrations[14] Another aspect of CODH function is the maturation of the enzyme, which involves the correct insertion of Ni and Fe into the active site[40]. CO in the Earth’s atmosphere, though between 50 and 160 ppb, is increasing regionally in the areas with large-scale anthropogenic inputs[3] In addition to these cultured members, molecular analysis of thermal environments has indicated that carboxydotrophic metabolisms and CO-related genes are commonplace in these thermal settings. Biosensors with COinert electrodes combined with immobilized CO oxidoreductase from the thermophile Pseudomonas thermocarboxovorans using phenazine ethosulfate as the electron acceptor (with a Km of 3.8 μM) have shown potential for CO detection within the ppm to ppb range with durability and rapid response[57]
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