title: Structural and oxidation state changes of the photosystem II manganese complex in four transitions of the water oxidation cycle (S0 --> S1, S1 --> S2, S2 --> S3, and S3,4 --> S0) characterized by X-ray absorption spectroscopy at 20 K and room temperature.
abstract: Structural and electronic changes (oxidation states) of the Mn(4)Ca complex of photosystem II (PSII) in the water oxidation cycle are of prime interest. For all four transitions between semistable S-states (S(0) --> S(1), S(1) --> S(2), S(2) --> S(3), and S(3),(4) --> S(0)), oxidation state and structural changes of the Mn complex were investigated by X-ray absorption spectroscopy (XAS) not only at 20 K but also at room temperature (RT) where water oxidation is functional. Three distinct experimental approaches were used: (1) illumination-freeze approach (XAS at 20 K), (2) flash-and-rapid-scan approach (RT), and (3) a novel time scan/sampling-XAS method (RT) facilitating particularly direct monitoring of the spectral changes in the S-state cycle. The rate of X-ray photoreduction was quantitatively assessed, and it was thus verified that the Mn ions remained in their initial oxidation state throughout the data collection period (>90%, at 20 K and at RT, for all S-states). Analysis of the complete XANES and EXAFS data sets (20 K and RT data, S(0)-S(3), XANES and EXAFS) obtained by the three approaches leads to the following conclusions. (i) In all S-states, the gross structural and electronic features of the Mn complex are similar at 20 K and room temperature. There are no indications for significant temperature-dependent variations in structure, protonation state, or charge localization. (ii) Mn-centered oxidation likely occurs on each of the three S-state transitions, leading to the S(3) state. (iii) Significant structural changes are coupled to the S(0) --> S(1) and the S(2) --> S(3) transitions which are identified as changes in the Mn-Mn bridging mode. We propose that in the S(2) --> S(3) transition a third Mn-(mu-O)(2)-Mn unit is formed, whereas the S(0) --> S(1) transition involves deprotonation of a mu-hydroxo bridge. In light of these results, the mechanism of accumulation of four oxidation equivalents by the Mn complex and possible implications for formation of the O-O bond are considered.
authors.affiliation: FB Physik, Freie Universität Berlin, Arnimallee 14, D-14195 Berlin, Germany. haumann@physik.fu-berlin.de
authors.forename: M
authors.initials: M
authors.lastname: Haumann
authors.forename: C
authors.initials: C
authors.lastname: Müller
authors.forename: P
authors.initials: P
authors.lastname: Liebisch
authors.forename: L
authors.initials: L
authors.lastname: Iuzzolino
authors.forename: J
authors.initials: J
authors.lastname: Dittmer
authors.forename: M
authors.initials: M
authors.lastname: Grabolle
authors.forename: T
authors.initials: T
authors.lastname: Neisius
authors.forename: W
authors.initials: W
authors.lastname: Meyer-Klaucke
authors.forename: H
authors.initials: H
authors.lastname: Dau
mesh_terms: D005615:Freezing; D008345:Manganese / Q000737:chemistry* / Q000378:metabolism; D010084:Oxidation-Reduction; D010782:Photolysis; D045332:Photosystem II Protein Complex / Q000737:chemistry* / Q000378:metabolism; D013057:Spectrum Analysis / Q000379:methods; D018724:Spinacia oleracea; D013329:Structure-Activity Relationship; D013696:Temperature; D014867:Water / Q000737:chemistry* / Q000378:metabolism; D014965:X-Rays
chemical_list: D045332:Photosystem II Protein Complex; D014867:Water; D008345:Manganese