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

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 (S-0-S-4) 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 S-1 and S-2 states. The proposed model consists of two di-mu-oxo-bridged binuclear Mn units with Mn-Mn distances of similar to 2.7 Angstrom that are linked to each other by a mono-mu-oxo bridge with a Mn-Mn separation of similar to 3.3 Angstrom. The Mn-Mn distances are invariant in the native S-1 and S-2 states. This report describes the application of X-ray absorption spectroscopy to S-3 samples created under physiological conditions with saturating flash illumination. Significant changes are observed in the Mn-Mn distances in the S-3 State compared to the S-1 and the S-2 states. The two 2.7 Angstrom Mn-Mn distances that characterize the di-mu-oxo centers in the S-1 and S-2 states are lengthened to similar to 2.8 and 3.0 Angstrom in the S-3 state, respectively. The 3.3 Angstrom Mn-Mn and Mn-Ca distances also increase by 0.04-0.2 Angstrom. These changes in Mn-Mn distances are interpreted as consequences of the onset of substrate/water oxidation in the S-3 state. Mn-centered oxidation is evident during the S-0-->S-1 and S-1-->S-2 transitions. We propose that the changes in Mn-Mn distances during the S-2-->S-3 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 S-3 state and the implications for the mechanism of water oxidation are discussed.