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

Inspecting S states in photosynthesis Oxygenic photosynthesis uses a Mn4CaO5 cluster in the oxygen-evolving complex to extract electrons from water and produce dioxygen. Visualizing each of the chemical states in this process, S0 to S4, and assigning chemical identities and mechanisms on the basis of structures has been a challenge addressed recently by work at x-ray free-electron lasers. Suga et al. used serial crystallography at cryogenic temperatures to trap and determine the structures of several stable states during photosystem II water oxidation (see the Perspective by Britt and Marchiori). Changes around the water cluster already happen in the S2 state and set the stage for water insertion that occurs during transition to the S3 state. A short 1.9-angstrom distance between the two oxygen atoms in the S3 state is consistent with theoretical studies supporting an oxyl/oxo mechanism for oxygen-oxygen coupling. Science, this issue p. 334; see also p. 305 Structures of photosystem II captured at an x-ray free-electron laser reveal details of photosynthetic oxygen evolution. Photosynthetic water oxidation is catalyzed by the Mn4CaO5 cluster of photosystem II (PSII) with linear progression through five S-state intermediates (S0 to S4). To reveal the mechanism of water oxidation, we analyzed structures of PSII in the S1, S2, and S3 states by x-ray free-electron laser serial crystallography. No insertion of water was found in S2, but flipping of D1 Glu189 upon transition to S3 leads to the opening of a water channel and provides a space for incorporation of an additional oxygen ligand, resulting in an open cubane Mn4CaO6 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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