Anoxygenic photosynthesis and the delayed oxygenation of Earth's atmosphere

Abstract: The emergence of oxygenic photosynthesis created a new niche with dramatic potential to transform energy flow through Earth's biosphere. However, more primitive forms of photosynthesis that fix CO2 into biomass using electrons from reduced species like Fe(II) and H2 instead of water would have competed with Earth's early oxygenic biosphere for essential nutrients. Here, we combine experimental microbiology, genomic analyses, and Earth system modeling to demonstrate that competition for light and nutrients in the surface ocean between oxygenic phototrophs and Fe(II)-oxidizing, anoxygenic photosynthesizers (photoferrotrophs) translates into diminished global photosynthetic O2 release when the ocean interior is Fe(II)-rich. These results provide a simple ecophysiological mechanism for inhibiting atmospheric oxygenation during Earth's early history. We also find a novel positive feedback within the coupled C-P-O-Fe cycles that can lead to runaway planetary oxygenation as rising atmospheric pO2 sweeps the deep ocean of the ferrous iron substrate for photoferrotrophy.