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

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-<i>μ</i>-oxo-bridged binuclear Mn units with Mn-Mn distances of ~2.7 Å that are linked to each other by a mono-<i>μ</i>-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-<i>μ</i>-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.