Structural Change of the Mn Cluster during the S2→S3 State Transition of the Oxygen-Evolving Complex of Photosystem II. Does It Reflect the Onset of Water/Substrate Oxidation? Determination by Mn X-ray Absorption Spectroscopy

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Abstract
The oxygen-evolving complex of Photosystem II in plants and cyanobacteria catalyzes the oxidation of two water molecules to one molecule of dioxygen. A tetranuclear Mn complex is believed to cycle through five intermediate states (S0−S4) to couple the four-electron oxidation of water with the one-electron photochemistry occurring at the Photosystem II reaction center. We have used X-ray absorption spectroscopy to study the local structure of the Mn complex and have proposed a model for it, based on studies of the Mn K-edges and the extended X-ray absorption fine structure of the S1 and S2 states. The proposed model consists of two di-μ-oxo-bridged binuclear Mn units with Mn−Mn distances of ∼2.7 Å that are linked to each other by a mono-μ-oxo bridge with a Mn−Mn separation of ∼3.3 Å. The Mn−Mn distances are invariant in the native S1 and S2 states. This report describes the application of X-ray absorption spectroscopy to S3 samples created under physiological conditions with saturating flash illumination. Significant changes are observed in the Mn−Mn distances in the S3 state compared to the S1 and the S2 states. The two 2.7 Å Mn−Mn distances that characterize the di-μ-oxo centers in the S1 and S2 states are lengthened to ∼2.8 and 3.0 Å in the S3 state, respectively. The 3.3 Å Mn−Mn and Mn−Ca distances also increase by 0.04−0.2 Å. These changes in Mn−Mn distances are interpreted as consequences of the onset of substrate/water oxidation in the S3 state. Mn-centered oxidation is evident during the S0→S1 and S1→S2 transitions. We propose that the changes in Mn−Mn distances during the S2→S3 transition are the result of ligand or water oxidation, leading to the formation of an oxyl radical intermediate formed at a bridging or terminal position. The reaction of the oxyl radical with OH-, H2O, or an oxo group during the subsequent S state conversion is proposed to lead to the formation of the O−O bond. Models that can account for changes in the Mn−Mn distances in the S3 state and the implications for the mechanism of water oxidation are discussed.