Mechanism of protonation of the over-reduced Mn4CaO5 cluster in photosystem II

Abstract

Based on characterization by X-ray absorption spectroscopy, it has been proposed that the Mn4CaO5 cluster in the crystal structure of the water-oxidizing enzyme, photosystem II (PSII), may represent an over-reduced form arising from reduction by the X-ray beam. Using a quantum mechanical/molecular mechanical approach, and assuming that all of the μ-oxo bridges are deprotonated in S1, we analyzed the reduction process of the Mn4CaO5 cluster. In the crystal structure, the O atom (O5), which is linked with three Mn atoms and one Ca atom, has no H-bond. When reduced to S–2, unexpectedly, a water molecule at Ca2+ (W3) reoriented itself, formed a H-bond with O5, and released a proton to O5, resulting in formation of OH− at both W3 and O5. Once generated, the OH− group at O5 was stable, because the W3…O5 H-bond had already disappeared. A weak binding of H2O at Ca2+ led W3 to reorient and serve as a proton donor to O5 upon over-reduction.