Oxidative adaptations in prokaryotes imply the oxygenic photosynthesis before crown-group Cyanobacteria

The metabolic transition from anaerobic to aerobic in prokaryotes reflects adaptations to oxidative stress. Methanogen, one of the earliest life forms on Earth, has evolved into three major groups within the Euryarchaeota, exhibiting different phylogenetic affiliations and metabolic characters. In comparison with other strictly anaerobic methanogenic groups, the Class II methanogens possess a better capability to adapt to limited oxygen pressure. Cyanobacteria is considered the first and only prokaryote evolving oxygenic photosynthesis and is responsible for the Great Oxidation Event on Earth. However, the connection between oxygenic Cyanobacteria and evolutionary adaptations to oxidative stress in prokaryotes remains elusive. Here, through the gene encoding structural maintenance of chromosomes (SMC) protein, which was horizontally transferred from ancient Class II methanogens to the last common ancestor of the crown-group Cyanobacteria, we demonstrate that the origin of extant Cyanobacteria was undoubtedly posterior to the occurrence of oxygen-tolerant Class II methanogens. In addition, we found that certain prokaryotic lineages had evolved the tolerance mechanisms against oxidative stress before the origin of extant Cyanobacteria. The contradiction that oxidative adaptations in Class II methanogens and other prokaryotes predating the crown-group oxygenic Cyanobacteria implies the existence of more ancient biological oxygenesis. We propose that these potential oxygenic organisms might represent the extinct phototrophs and first emerge during the Paleoarchean, contributing to the oxidative adaptations in the prokaryotic tree of life and facilitating the dispersal of reaction centers across the bacterial domain.