  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.
