Due to fierce competition for resources, soil bacteria are often starved of energy sources like organic carbon. To cope with this, many bacteria have evolved to persist using alternative energy sources including the trace quantities of carbon monoxide (CO) present in the atmosphere. To do this, they utilise high-affinity variants of the enzyme molybdenum-copper carbon monoxide dehydrogenase (MoCu-CODH). To understand this process, we isolated the high-affinity MoCu-CODH from the soil bacterium Mycobacterium smegmatis and determined the structure at 1.85 Å resolution using Cryo-EM. We found that MoCu-CODH is a soluble enzyme with no membrane-associated regions. However, to provide energy to the cell via respiration it must transfer electrons derived from CO to the hydrophobic electron transport molecule menaquinone, which is localised in the cell membrane. We used X-ray crystallography to determine the structure of an uncharacterised lipid-anchored protein CoxG, an accessory protein found in the MoCu-CODH operon, previously implicated in the localisation of MoCu-CODH to the cell membrane. We show that CoxG contains a hydrophobic cavity, which specifically binds menaquinone in M. smegmatis. AlphaFold2 modelling demonstrated that CoxG binds to MoCu-CODH within proximity of MoCu-CODH’s FAD group, the terminal point of electron transfer from CO oxidation in MoCu-CODH. M. smegmatis cells lacking CoxG can no longer oxidise CO, however when supplemented with an artificial electron acceptor, MoCu-CODH regains activity. We hypothesise that CoxG shuttles menaquinone from the membrane to MoCu-CODH, where it is reduced with electrons from atmospheric CO. Subsequently, CoxG returns reduced menaquinol to the membrane where it is utilised by the respiratory chain for eventual ATP production.