Primary Productivity Was Limited by Electron Donors Prior to the Advent of Oxygenic Photosynthesis

Abstract

To evaluate productivity on the early Earth before the advent of oxygenic photosynthesis, we integrated estimates of net primary production by early anaerobic metabolisms as limited by geological fluxes of key electron donor compounds, phosphate, and fixed nitrogen. These calculations show that productivity was limited by fluxes of electron donor compounds to rates that were orders of magnitude lower than today. Results suggest that ferrous iron provided a minor fuel for net primary productivity compared to molecular hydrogen. Fluxes of fixed nitrogen and phosphate were in excess of demands by the electron donor-limited biosphere, even without biological nitrogen fixation. This suggests that until life learned to use water as an electron donor for photosynthesis, the size and productivity of the biosphere were constrained by the geological supply of electron donors and there may not have been much ecological pressure to evolve biological nitrogen fixation. Moreover, extremely low productivity in the absence of oxygenic photosynthesis has implications for the potential scale of biospheres on icy worlds such as Enceladus and Europa, where photosynthesis is not possible and life would be unable to escape electron donor limitation.