EVOLUTION OF CYTOCHROME-OXIDASE, AN ENZYME OLDER THAN ATMOSPHERIC OXYGEN

Cytochrome oxidase is a key enzyme in aerobic metabolism. All the reco rded eubacterial (domain Bacteria) and archaebacterial (Archaea) seque nces of subunits 1 and 2 of this protein complex have been used for a comprehensive evolutionary analysis. The phylogenetic trees reveal sev eral processes of gene duplication. Some of these are ancient, having occurred in the common ancestor of Bacteria and Archaea, whereas other s have occurred in specific lines of Bacteria. We show that eubacteria l quinol oxidase was derived from cytochrome c oxidase in Gram-positiv e bacteria and that archaebacterial quinol oxidase has an independent origin. A considerable amount of evidence suggests that Proteobacteria (Purple bacteria) acquired quinol oxidase through a lateral gene tran sfer from Gram-positive bacteria. The prevalent hypothesis that aerobi c metabolism arose several times in evolution after oxygenic photosynt hesis, is not sustained by two aspects of the molecular data. First, c ytochrome oxidase was present in the common ancestor of Archaea and Ba cteria whereas oxygenic photosynthesis appeared in Bacteria. Second, a n extant cytochrome oxidase in nitrogen-fixing bacteria shows that aer obic metabolism is possible in an environment with a very low level of oxygen, such as the root nodules of leguminous plants. Therefore, we propose that aerobic metabolism in organisms with cytochrome oxidase h as a monophyletic and ancient origin, prior to the appearance of eubac terial oxygenic photosynthetic organisms.