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 stressinsomeorganismsasaresultofreactionsbetweenFe(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 cyanobacteriadecreasedboththeeci encyofoxygenicphotosynthesis 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 oxygenationwascontrolledbythetimingofsubmarine,plumetype volcanism, with Fe(II) toxicity as the modulating factor. Possible biological explanations for the slow tempo of atmospheric oxidation invoke limitations on the efficiency of early oxygenic photosynthesis, such as the toxicity of oxygen to the organisms who first produced it 7 , or that a paucity of key nutrients limited growth of oxygenic phototrophs in late Archaean sea water 8 . Iron is a key limiting nutrient for oxygenic photosynthesis in modern, oxic oceans, and enhanced Fe fluxes to the surface ocean are generally thought to have increased primary productivity over geologic time 9 . Coastal environments in the late Archaean experienced enhanced fluxes of Fe in its reduced, soluble form (Fe(II)) from upwelling sea water saturated with Fe(II) supplied from hydrothermal leaching of oceanic crust 10,11 . In the absence of land plants in the late Archaean, a reasonable assumption is that most oxygen was produced or built up locally in coastal marine environments that experienced such upwelling 5,12 , and oxygenic phototrophs would have experienced these Fe(II) fluxes. Nearly half of Earth’s primary productivity, and hence its oxygen production, is today produced in the oceans 13 , and planktonic marine cyanobacteria, such as Synechococcus and Prochlorococcus, account for up to 25% of this number 14 . As previous work documented significant oxidative stress when planktonic cyanobacteria were