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

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Abstract
Structural and electronic changes (oxidation states) of the Mn4Ca complex of photosystem II (PSII) in the water oxidation cycle are of prime interest. For all four transitions between semistable S-states (S0 → S1, S1 → S2, S2 → S3, and S3,4 → S0), 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, S0−S3, 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 S3 state. (iii) Significant structural changes are coupled to the S0 → S1 and the S2 → S3 transitions which are identified as changes in the Mn−Mn bridging mode. We propose that in the S2 → S3 transition a third Mn−(μ-O)2−Mn unit is formed, whereas the S0 → S1 transition involves deprotonation of a μ-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.

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