Modulation of oxygen production in Archaean oceans by episodes of Fe(II) toxicity

Oxygen accumulated in the surface waters of the Earth's oceans(1) and atmosphere(2) several hundred million years before the Great Oxidation Event between 2.4 and 2.3 billion years ago(3). Before the Great Oxidation Event, periods of enhanced submarine volcanism associated with mantle plume events(4) supplied Fe(II) to sea water. These periods generally coincide with the disappearance of indicators of the presence of molecular oxygen in Archaean sedimentary records(5). The presence of Fe(II) in the water column can lead to oxidative stress in some organisms as a result of reactions between Fe(II) and oxygen that produce reactive oxygen species(6). Here we test the hypothesis that the upwelling of Fe(II)-rich, anoxic water into the photic zone during the late Archaean subjected oxygenic phototrophic bacteria to Fe(II) toxicity. In laboratory experiments, we found that supplying Fe(II) to the anoxic growth medium housing a common species of planktonic cyanobacteria decreased both the efficiency of oxygenic photosynthesis and their growth rates. We suggest that this occurs because of increasing intracellular concentrations of reactive oxygen species. We use geochemical modelling to show that Fe(II) toxicity in conditions found in the late Archaean photic zone could have substantially inhibited water column oxygen production, thus decreasing fluxes of oxygen to the atmosphere. We therefore propose that the timing of atmospheric oxygenation was controlled by the timing of submarine, plume-type volcanism, with Fe(II) toxicity as the modulating factor.