Anoxygenic photosynthesis and the delayed oxygenation of Earth\u2019s atmosphere

Kazumi Ozaki,Katharine J Thompson,Rachel L Simister,Sean A Crowe,Christopher T Reinhard

doi:10.1038/s41467-019-10872-z

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.

Highlights

The emergence of oxygenic photosynthesis created a new niche with dramatic potential to transform energy flow through Earth’s biosphere
Anoxygenic phototrophs proliferate in sunlit anoxic environments where they utilize a wide-range of electron donors including dihydrogen, hydrogen sulfide, thiosulphate, elemental sulfur, and ferrous iron [Fe(II)]12
Ferrous iron would have been the most widely available electron donor for anoxygenic photosynthesis throughout much of Earth’s early history[13,14,15,16,17,18,19,20,21,22], but the birth of the oxygen-evolving complex in the ancestors of extant cyanobacteria would have created a new photosynthetic niche decoupled from the supply of Fe(II) to illuminated surface ocean waters

Summary

Introduction

The emergence of oxygenic photosynthesis created a new niche with dramatic potential to transform energy flow through Earth’s biosphere. Ferrous iron would have been the most widely available electron donor for anoxygenic photosynthesis throughout much of Earth’s early history[13,14,15,16,17,18,19,20,21,22], but the birth of the oxygen-evolving complex in the ancestors of extant cyanobacteria would have created a new photosynthetic niche decoupled from the supply of Fe(II) to illuminated surface ocean waters This would have initiated fierce competition for light and bioessential elements—most importantly phosphorus (P)[23,24,25,26,27]. In the modern ocean and many lakes, for example, lowlight-adapted phytoplankton inhabit deep chlorophyll maxima, where they exploit nutrient supplies from below, make large contributions to primary production, and strongly diminish nutrient fluxes to the upper photic zone[29]

Methods

Results

Conclusion