title: Room-Temperature Energy-Sampling Kβ X-ray Emission Spectroscopy of the Mn4Ca Complex of Photosynthesis Reveals Three Manganese-Centered Oxidation Steps and Suggests a Coordination Change Prior to O2 Formation.
abstract: In oxygenic photosynthesis, water is oxidized and dioxygen is produced at a Mn4Ca complex bound to the proteins of photosystem II (PSII). Valence and coordination changes in its catalytic S-state cycle are of great interest. In room-temperature (in situ) experiments, time-resolved energy-sampling X-ray emission spectroscopy of the Mn Kβ1,3 line after laser-flash excitation of PSII membrane particles was applied to characterize the redox transitions in the S-state cycle. The Kβ1,3 line energies suggest a high-valence configuration of the Mn4Ca complex with Mn(III)3Mn(IV) in S0, Mn(III)2Mn(IV)2 in S1, Mn(III)Mn(IV)3 in S2, and Mn(IV)4 in S3 and, thus, manganese oxidation in each of the three accessible oxidizing transitions of the water-oxidizing complex. There are no indications of formation of a ligand radical, thus rendering partial water oxidation before reaching the S4 state unlikely. The difference spectra of both manganese Kβ1,3 emission and K-edge X-ray absorption display different shapes for Mn(III) oxidation in the S2 → S3 transition when compared to Mn(III) oxidation in the S1 → S2 transition. Comparison to spectra of manganese compounds with known structures and oxidation states and varying metal coordination environments suggests a change in the manganese ligand environment in the S2 → S3 transition, which could be oxidation of five-coordinated Mn(III) to six-coordinated Mn(IV). Conceivable options for the rearrangement of (substrate) water species and metal-ligand bonding patterns at the Mn4Ca complex in the S2 → S3 transition are discussed.
authors.affiliation: Freie Universität Berlin , Department of Physics, 14195 Berlin, Germany.
authors.forename: Ivelina
authors.initials: I
authors.lastname: Zaharieva
authors.affiliation: Freie Universität Berlin , Department of Physics, 14195 Berlin, Germany.
authors.forename: Petko
authors.initials: P
authors.lastname: Chernev
authors.affiliation: Uppsala University , Department of Chemistry, Ångström Laboratory, 75120 Uppsala, Sweden.
authors.forename: Gustav
authors.initials: G
authors.lastname: Berggren
authors.affiliation: Uppsala University , Department of Chemistry, Ångström Laboratory, 75120 Uppsala, Sweden.
authors.forename: Magnus
authors.initials: M
authors.lastname: Anderlund
authors.affiliation: Uppsala University , Department of Chemistry, Ångström Laboratory, 75120 Uppsala, Sweden.
authors.forename: Stenbjörn
authors.initials: S
authors.lastname: Styring
authors.affiliation: Freie Universität Berlin , Department of Physics, 14195 Berlin, Germany.
authors.forename: Holger
authors.initials: H
authors.lastname: Dau
authors.affiliation: Freie Universität Berlin , Department of Physics, 14195 Berlin, Germany.
authors.forename: Michael
authors.initials: M
authors.lastname: Haumann
mesh_terms: D002118:Calcium / Q000737:chemistry; D007700:Kinetics; D008345:Manganese / Q000737:chemistry*; D008956:Models, Chemical; D008958:Models, Molecular; D010084:Oxidation-Reduction; D010100:Oxygen / Q000378:metabolism; D010788:Photosynthesis; D045332:Photosystem II Protein Complex / Q000737:chemistry* / Q000378:metabolism*; D013052:Spectrometry, X-Ray Emission; D018724:Spinacia oleracea / Q000378:metabolism; D013696:Temperature
chemical_list: D045332:Photosystem II Protein Complex; D008345:Manganese; D010100:Oxygen; D002118:Calcium