title: Structural Change of the Mn Cluster during the S2→S3State 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 S1and S2states. 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 S1and S2states. This report describes the application of X-ray absorption spectroscopy to S3samples created under physiological conditions with saturating flash illumination. Significant changes are observed in the Mn-Mn distances in the S3state compared to the S1and the S2states. The two 2.7 Å Mn-Mn distances that characterize the di-μ-oxo centers in the S1and S2states are lengthened to ~2.8 and 3.0 Å in the S3state, 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 S3state. Mn-centered oxidation is evident during the S0→S1and S1→S2transitions. We propose that the changes in Mn-Mn distances during the S2→S3transition 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 S3state and the implications for the mechanism of water oxidation are discussed.
authors.affiliation: Melvin Calvin Laboratory, Physical Biosciences Division, Lawrence Berkeley National Laboratory, and Department of Chemistry, University of California, Berkeley, California 94720-5230.
authors.forename: Wenchuan
authors.initials: W
authors.lastname: Liang
authors.affiliation: Melvin Calvin Laboratory, Physical Biosciences Division, Lawrence Berkeley National Laboratory, and Department of Chemistry, University of California, Berkeley, California 94720-5230.
authors.forename: Theo A
authors.initials: TA
authors.lastname: Roelofs
authors.affiliation: Melvin Calvin Laboratory, Physical Biosciences Division, Lawrence Berkeley National Laboratory, and Department of Chemistry, University of California, Berkeley, California 94720-5230.
authors.forename: Roehl M
authors.initials: RM
authors.lastname: Cinco
authors.affiliation: Melvin Calvin Laboratory, Physical Biosciences Division, Lawrence Berkeley National Laboratory, and Department of Chemistry, University of California, Berkeley, California 94720-5230.
authors.forename: Annette
authors.initials: A
authors.lastname: Rompel
authors.affiliation: Melvin Calvin Laboratory, Physical Biosciences Division, Lawrence Berkeley National Laboratory, and Department of Chemistry, University of California, Berkeley, California 94720-5230.
authors.forename: Matthew J
authors.initials: MJ
authors.lastname: Latimer
authors.affiliation: Melvin Calvin Laboratory, Physical Biosciences Division, Lawrence Berkeley National Laboratory, and Department of Chemistry, University of California, Berkeley, California 94720-5230.
authors.forename: Wa O
authors.initials: WO
authors.lastname: Yu
authors.affiliation: Melvin Calvin Laboratory, Physical Biosciences Division, Lawrence Berkeley National Laboratory, and Department of Chemistry, University of California, Berkeley, California 94720-5230.
authors.forename: Kenneth
authors.initials: K
authors.lastname: Sauer
authors.affiliation: Melvin Calvin Laboratory, Physical Biosciences Division, Lawrence Berkeley National Laboratory, and Department of Chemistry, University of California, Berkeley, California 94720-5230.
authors.forename: Melvin P
authors.initials: MP
authors.lastname: Klein
authors.affiliation: Melvin Calvin Laboratory, Physical Biosciences Division, Lawrence Berkeley National Laboratory, and Department of Chemistry, University of California, Berkeley, California 94720-5230.
authors.forename: Vittal K
authors.initials: VK
authors.lastname: Yachandra