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 (O(2)Red), the key enzymes of aerobic respiratory chains. The distribution and phylogenetic analysis of the four types of O(2)Red (Cyt-bd and the A, B, and C families of heme-copper O(2)Red) 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-O(2)Red are of proteobacterial origin and were transferred to a few other bacteria; B-O(2)Red are of archaeal origin and were transferred to a few bacteria; and A-O(2)Red are the most ancient O(2)Red 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.