The electron–proton bottleneck of photosynthetic oxygen evolution

Paul Greife, Matthias Schönborn, Matteo Capone, Ricardo Assunção, Daniele Narzi, Leonardo Guidoni () and Holger Dau ()
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Paul Greife: Freie Universität
Matthias Schönborn: Freie Universität
Matteo Capone: University of L’Aquila
Ricardo Assunção: Freie Universität
Daniele Narzi: University of L’Aquila
Leonardo Guidoni: University of L’Aquila
Holger Dau: Freie Universität

Nature, 2023, vol. 617, issue 7961, 623-628

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41586-023-06008-5

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