Abstract

The evolution of oxygenic photosynthesis is a pivotal event in Earth’s history because the O2 released fundamentally changed the planet’s redox state and facilitated the emergence of multicellular life. An intriguing hypothesis proposes that hydrogen peroxide (H2O2) once acted as the electron donor prior to the evolution of oxygenic photosynthesis, but its abundance during the Archean would have been limited. Here, we report a previously unrecognized abiotic pathway for Archean H2O2 production that involves the abrasion of quartz surfaces and the subsequent generation of surface-bound radicals that can efficiently oxidize H2O to H2O2 and O2. We propose that in turbulent subaqueous environments, such as rivers, estuaries and deltas, this process could have provided a sufficient H2O2 source that led to the generation of biogenic O2, creating an evolutionary impetus for the origin of oxygenic photosynthesis.

Highlights

  • The evolution of oxygenic photosynthesis is a pivotal event in Earth’s history because the O2 released fundamentally changed the planet’s redox state and facilitated the emergence of multicellular life

  • Oxygenic photosynthesis operates by a four-electron reaction (R1) process associated with chlorophyll-a and the water-oxidizing complex (WOC)[1,2]

  • As an early intermediate candidate prior to H2O, H2O2 is plausible for two reasons. It can be oxidized at electrochemical potentials that are accessible to existing anoxygenic phototrophs[1], meaning that if photosynthesis evolved as an anoxygenic process, as is generally accepted[9], the photosynthetic machinery might already have been in place to handle H2O2 redox transformations

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Summary

Introduction

The evolution of oxygenic photosynthesis is a pivotal event in Earth’s history because the O2 released fundamentally changed the planet’s redox state and facilitated the emergence of multicellular life. The evolution of oxygenic photosynthesis was a critical biological innovation that allowed water to be used as an electron source and dioxygen gas (O2) to be released as a metabolic by-product to the early atmosphere. Oxygenic photosynthesis operates by a four-electron reaction (R1) process associated with chlorophyll-a and the water-oxidizing complex (WOC)[1,2].

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