Nitrogenase inhibition limited oxygenation of the Proterozoic atmosphere

Cyanobacteria produced the atmospheric O2 that began accumulating 2.4 billion years ago1, leading to Earths Great Oxidation Event (GOE)2. For nearly 2 billion years following the GOE, O2 production was restricted and atmospheric oxygen remained low2-5. Oxygen rose again sharply with the advent of land plants roughly 450 million years ago, which increased atmospheric O2 through carbon burial4-5. Why did the O2 content of the atmosphere remain constant and low for more than a billion years despite the existence of O2-producing cyanobacteria? While geological limitations have been explored2-7, 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 volume8. No O2-resistant nitrogenase enzyme is known9-12. 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.