Nitrogenase inhibition limited oxygenation of the Proterozoic atmosphere

Cyanobacteria produced the atmospheric O2 that began accumulating 2.4 billion years ago, leading to Earth9s Great Oxidation Event (GOE). For nearly two billion years following the GOE, O2 production was restricted and atmospheric oxygen remained low. Oxygen rose again sharply with the advent of land plants roughly 450 million years ago, which increased atmospheric O2 through carbon burial. Why did the O2 content of the atmosphere remain constant and low for more than a billion years despite the existence of O2-producng cyanobacteria? While geological limitations have been explored, the limiting factor may have been biological, and enzymatic. Here we propose that O2 was kept low by oxygen inhibition of nitrogenase activity. Nitrogenase is the sole N2-fixing enzyme on Earth, and is inactive in air containing 2% or more O2 by volume. No O2-resistant nitrogenase is known. We further propose that nitrogenase inhibition by O2 kept atmospheric O2 low until upright terrestrial plants physically separated O2 production in aerial photosynthetic tissues from N2 fixation in soil, liberating nitrogenase from inhibition by atmospheric O2.