Abstract

Cyanobacteria produced the oxygen that began to accumulate on Earth 2.5 billion years ago, at the dawn of the Proterozoic Eon. By 2.4 billion years ago, the Great Oxidation Event (GOE) marked the onset of an atmosphere containing oxygen. The oxygen content of the atmosphere then remained low for almost 2 billion years. Why? Nitrogenase, the sole nitrogen-fixing enzyme on Earth, controls the entry of molecular nitrogen into the biosphere. Nitrogenase is inhibited in air containing more than 2% oxygen: the concentration of oxygen in the Proterozoic atmosphere. We propose that oxygen inhibition of nitrogenase limited Proterozoic global primary production. Oxygen levels increased when upright terrestrial plants isolated nitrogen fixation in soil from photosynthetic oxygen production in shoots and leaves.

Highlights

  • Oxygen gas is a classic example of life changing Earth: from a fully inhabited but anoxic planet to today’s green, rich biosphere in an atmosphere containing 21% O2 by volume

  • Following the Great Oxidation Event (GOE), O2 rose to only 10% of its present atmospheric level (PAL), and stayed there for most of the Proterozoic

  • Geochemical evidence suggests that the oceans remained largely anoxic throughout the Proterozoic [4,12,16], with a rise to modern oxygen levels starting around 580 million years (MY) ago [18] and in deep oceans perhaps as recently as only 430 MY ago [19] (Figure 1)

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Summary

Trends in Plant Science

Cyanobacteria produced the oxygen that began to accumulate on Earth 2.5 billion years ago, at the dawn of the Proterozoic Eon. In the Proterozoic ‘boring billion’, oxygen inhibited nitrogen fixation, cell growth, and photosynthesis on a global scale, suppressing any further rise in atmospheric oxygen until the arrival of land plants about 450 million years ago. The cooperation of two distinct types of photochemical reaction centre at the origin of water-splitting, oxygenic photosynthesis 2.5 billion years ago fundamentally changed the nature of primary production: the novel reductant, water, could never be limiting in aquatic environments. Nitrogenase Is an Autoregulator of Oxygen Levels Here we propose Proterozoic limitation of primary production by a macronutrient: fixed nitrogen. Nitrogen fixation is inhibited by molecular oxygen [32,43,55,56,57,58] in the feedback loop depicted in Figure 3 (Key Figure) We propose that this simple property alone limited O2 accumulation over geological time.

Inhibitory Feedback at Nitrogenase
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