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Photosystem II Acts as a Spin-Controlled Electron Gate during Oxygen Formation and Evolution.

The oxygen evolution complex (OEC) of photosystem II (PSII) is intrinsically more active than any synthetic alternative for the oxygen evolution reaction (OER). A crucial question to solve for the progress of artificial photosynthesis is to understand the influential interactions during water oxidation in PSII. We study the principles of interatomic electron transfer steps in OER, with emphasis on exchange interactions, revealing the influence of delocalizing ferromagnetic spin potentials during the catalytic process. The OEC is found to be an exchange coupled mixed-valence electron-spin acceptor where its orbital physics determine the unique activity of PSII. The two unpaired electrons needed in the triplet O2 molecule interact with the high spin state of the catalyst via exchange interactions; the optimal ferromagnetic catalyst and the resulting radical intermediates are spin paired. As a result, the active center of the CaMn4O5 cofactor, stimulated by the driving potential provided by photons, works as a spin valve to accelerate the formation and release of O2 from diamagnetic H2O.