What computational chemistry and magnetic resonance reveal concerning the oxygen evolving centre in Photosystem II.

Density Functional Theory (DFT) computational studies of the Mn4/Ca Oxygen Evolving Complex (OEC) region of Photosystem II in the paramagnetic S2 and S3 states of the water oxdizing catalytic cycle are described. These build upon recent advances in computationally understanding the detailed S1 state OEC geometries, revealed by the recent high resolution Photosystem II crystal structures of Shen et al., at 1.90Å and 1.95Å (Petrie et al., 2015, Angew. Chem. Int. Ed., 54, 7120). The models feature a ‘Low Oxidation Paradigm’ assumption for the mean Mn oxidation states in the functional enzyme, with the mean oxidation levels being 3.0, 3.25 and 3.5 in S1, S2 and S3, respectively. These calculations are used to infer magnetic exchange interactions within the coupled OEC cluster, particularly in the Electron Paramagnetic Resonance (EPR)-visible S2 and S3 states. Detailed computational estimates of the intrinsic magnitudes and molecular orientations of the 55Mn hyperfine tensors in the S2 state are presented. These parameters, together with the resultant spin projected hyperfine values are compared with recent appropriate experimental EPR data (Continuous Wave (CW), Electron-Nuclear Double Resonance (ENDOR) and ELDOR (Electron-Electron Double Resonance)-Detected Nuclear Magnetic Resonance (EDNMR)) from the OEC. It is found that an effective Coupled Dimer magnetic organization of the four Mn in the OEC cluster in the S2 and S3 states is able to quantitatively rationalize the observed 55Mn hyperfine data. This is consistent with structures we propose to represent the likely state of the OEC in the catalytically active form of the enzyme.