An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser.

Photosynthetic water oxidation is catalyzed by the Mn ₄ CaO ₅ cluster of photosystem II (PSII) with linear progression through five S-state intermediates (S ₀ to S ₄ ). To reveal the mechanism of water oxidation, we analyzed structures of PSII in the S ₁ , S ₂ , and S ₃ states by x-ray free-electron laser serial crystallography. No insertion of water was found in S ₂ , but flipping of D1 Glu ¹⁸⁹ upon transition to S ₃ leads to the opening of a water channel and provides a space for incorporation of an additional oxygen ligand, resulting in an open cubane Mn ₄ CaO ₆ cluster with an oxyl/oxo bridge. Structural changes of PSII between the different S states reveal cooperative action of substrate water access, proton release, and dioxygen formation in photosynthetic water oxidation.
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