Oxygen reductase origin followed the great oxidation event and terminated the Lomagundi excursion

The history of Earth's atmospheric oxygen is a cornerstone of evolutionary biology. While unequivocal evidence for an increase in atmospheric O₂ marks the Great Oxidation Event (GOE) roughly 2.4 billion years ago, evidence underlying proposals for pre-GOE O₂ accumulation is debated. Here we have investigated the distribution of genes for oxygen reductases, the enzymes that consume O₂ in respiratory chains, across independently generated molecular timescales of prokaryotic evolution. The data indicate that cytochrome bd-oxidases, heme-copper oxidases and alternative oxidases arose in the wake of the GOE ca. 2.4 billion years ago, after which the genes were subjected to abundant lateral gene transfer, a reflection of their utility in redox balance and membrane bioenergetics. The data lead us to propose a straightforward four-stage model for O₂ accumulation surrounding the GOE: (i) Negligible O₂ existed prior to the GOE. (ii) Cyanobacterial O₂ production started at the GOE, yet was capped at 2 % [v/v] atmospheric O₂, the threshold at which cyanobacterial nitrogenase is inhibited by O₂. (iii) Production of 0.02 atm of O₂ (2 % [v/v]) at the GOE buried roughly the entire atmospheric CO₂ inventory, causing sudden enrichment of ¹³C in dissolved inorganic carbon (the Lomagundi ¹³C anomaly), through RuBisCO isotope discrimination, without atmospheric O₂ exceeding 2 % [v/v]. (iv) High atmospheric ¹²C at the end of the Lomagundi excursion marks the origin of oxygen reductases, their rapid spread via function in respiratory CO₂ liberation, and the onset of equilibrium between photosynthetic O₂ production and respiratory O₂ consumption at 2 % atmospheric O₂.