Electronic Structural Changes of Mn in the Oxygen-Evolving Complex of Photosystem II During the Catalytic Cycle

The oxygen evolving complex (OEC) in Photosystem II (PS II) was studied in the S0 through S3 states using 1s2p direct resonant inelastic X-ray scattering (RIXS) spectroscopy. The spectral changes of the OEC during the S-state transitions are subtle, indicating that the electrons are strongly delocalized throughout the cluster. The result suggests that in addition to the Mn ions ligands are also playing an important role in the redox reactions. A series of MnIV coordination complexes with different protonation states, nuclearity, and with and without the presence of Ca were compared, particularly with the PS II S3 state spectrum to understand its oxidation state. We find strong variations of the electronic structure within the series of MnIV model systems. The spectrum of the S3 state best resembles the MnIV complexes, Mn3IVCa2 and saplnMn2IV(OH)2, i.e. the oxo-bridge protonation of Mn dimer complexes and the presence of Ca in one corner of a Mn cubane structure show a similar spectroscopic response, suggesting that Ca in PS II and protonation of the oxo-bridge may give rise to analogous modifications of the electronic structure at the Mn sites. The current result emphasizes that the assignment of formal oxidation states alone is not sufficient for understanding the detailed electronic structural changes that govern the catalytic reaction in the OEC.