Heme A-containing oxidases evolved in the ancestors of iron oxidizing bacteria

The origin of oxygen respiration in bacteria has long intrigued biochemists, microbiologists and evolutionary biologists. The earliest enzymes that consume oxygen to extract energy did not evolve in the same lineages of photosynthetic bacteria that released oxygen on primordial earth, leading to the great oxygenation event (GOE). A widespread type of such enzymes is proton pumping cytochrome c oxidase (COX) that contains heme A, a unique prosthetic group for these oxidases. Here we show that the most ancestral proteins for the biosynthesis of heme A are present in extant acidophilic Fe2+-oxidizing Proteobacteria. Acidophilic Fe2+-oxidizers lived on emerged land around the time of the GOE, as suggested by the earliest geochemical evidence for aerobic respiration on paleoproterozoic earth. The gene for heme A synthase in acidophilic Fe2+-oxidizing Proteobacteria is associated with the COX gene cluster for iron oxidation. Compared to many other soil bacteria, the COX subunits encoded by this gene cluster are early diverging. Our data suggest that the ancient bacterial lineage which first evolved heme A-containing COX was related to the ancestors of present acidophilic Fe2+-oxidizers such as Acidiferrobacter and Acidithiobacillus spp. The copper leaching activity of such bacteria might have constituted a key ecological factor to promote COX evolution.