The Multiple Evolutionary Histories of Dioxygen Reductases: Implications for the Origin and Evolution of Aerobic Respiration

Understanding the origin and evolution of cellular processes is fundamental to understand how biological activity has shaped the history of our planet. Among these, aerobic respiration is probably one of the most debated. We have applied a phylogenomics approach to investigate the origin and evolution of dioxygen reductases (O2Red), the key enzymes of aerobic respiratory chains. The distribution and phylogenetic analysis of the four types of O2Red (Cyt-bd and the A, B, and C families of heme-copper O2Red) from 673 complete bacterial and archaeal genomes show that these enzymes have very different evolutionary histories: Cyt-bd are of bacterial origin and were transferred to a few archaea; C-O2Red are of proteobacterial origin and were transferred to a few other bacteria; B-O2Red are of archaeal origin and were transferred to a few bacteria; and A-O2Red are the most ancient O2Red and were already present prior to the divergence of major present-day bacterial and archaeal phyla, thus before the emergence of Cyanobacteria and oxygenic photosynthesis. Implications for the origin and the evolution of aerobic respiration are discussed.