The electron–proton bottleneck of photosynthetic oxygen evolution
Paul Greife, Matthias Schönborn, Matteo Capone, Ricardo Assunção, Daniele Narzi, Leonardo Guidoni, Holger Dau
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 S 4 state—which was postulated half a century ago 1 and remains largely uncharacterized. Here we resolve this key stage of photosynthetic O 2 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 O 2 formation, with a moderate energetic barrier and marked entropic slowdown. We identify the S 4 state as the oxygen-radical state; its formation is followed by fast O–O bonding and O 2 release. In conjunction with previous breakthroughs in experimental and computational investigations, a compelling atomistic picture of photosynthetic O 2 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.