The electron-proton bottleneck of photosynthetic oxygen evolution

Nature. 2023 May;617(7961):623-628. doi: 10.1038/s41586-023-06008-5. Epub 2023 May 3.

Abstract

Photosynthesis fuels life on Earth by storing solar energy in chemical form. Today's oxygen-rich atmosphere has resulted from the splitting of water at the protein-bound manganese cluster of photosystem II during photosynthesis. Formation of molecular oxygen starts from a state with four accumulated electron holes, the S4 state-which was postulated half a century ago1 and remains largely uncharacterized. Here we resolve this key stage of photosynthetic O2 formation and its crucial mechanistic role. We tracked 230,000 excitation cycles of dark-adapted photosystems with microsecond infrared spectroscopy. Combining these results with computational chemistry reveals that a crucial proton vacancy is initally created through gated sidechain deprotonation. Subsequently, a reactive oxygen radical is formed in a single-electron, multi-proton transfer event. This is the slowest step in photosynthetic O2 formation, with a moderate energetic barrier and marked entropic slowdown. We identify the S4 state as the oxygen-radical state; its formation is followed by fast O-O bonding and O2 release. In conjunction with previous breakthroughs in experimental and computational investigations, a compelling atomistic picture of photosynthetic O2 formation emerges. Our results provide insights into a biological process that is likely to have occurred unchanged for the past three billion years, which we expect to support the knowledge-based design of artificial water-splitting systems.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Electrons*
  • Oxidation-Reduction
  • Oxygen* / chemistry
  • Oxygen* / metabolism
  • Photosynthesis*
  • Photosystem II Protein Complex / chemistry
  • Photosystem II Protein Complex / metabolism
  • Protons*
  • Water / chemistry
  • Water / metabolism

Substances

  • Oxygen
  • Photosystem II Protein Complex
  • Protons
  • Water