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

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 K beta(1,3) line after laser-flash excitation of PSII membrane particles was applied to characterize the redox transitions in the S-state cycle. The K beta(1,3) line energies suggest a high-valence configuration of the Mn4Ca complex with Mn(III)(3)Mn(IV) in S-0, Mn(III)(2)Mn(IV)(2) in S-1, Mn(III)Mn(IV)(3) in S-2, and Mn(IV)(4) in S-3 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 S-4 state unlikely. The difference spectra of both manganese K beta(1,3) emission and K-edge X-ray absorption display different shapes for Mn(III) oxidation in the S-2 -> S-3 transition when compared to Mn(III) oxidation in the S-1 -> S-2 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 S-2 -> S-3 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 S-2 -> S-3 transition are discussed.