Structural and electronic models of the water oxidizing complex in the S₀ state of photosystem II: A density functional study

Large size (228 atom, 229 atom for protonated form) molecular models of the oxygen evolving complex of photosystem II (OEC), with a complete set of ligating aminoacids, the redox-active tyrosine Y_Z, and proton/water transfer channels terminating at the water oxidizing Mn/Ca cluster, are constructed based on the highest available resolution X-ray diffraction structures of the protein and our previous density functional theory (DFT) studies of isolated metal cluster model structures. Geometries optimized using the general gradient approximation (GGA) or hybrid density functionals are compared with high-resolution extended X-ray absorption fine structure (EXAFS) spectroscopic data and show that an antiferromagnetic configuration of the Mn centers in the cluster gives computed metal-metal distances in excellent agreement with experiment. The excitation energies predicted by time-dependent density functional theory (TDDFT) calculations for truncated 106 atom and 78 atom structures derived from the large models show that a previously proposed III-III-III-II oxidation pattern of the Mn atoms agrees very well with the X-ray absorption near-edge structure (XANES) observed for the S₀ state of the OEC. This supports a "low" Mn oxidation state paradigm for the OEC, when a realistic protein imposed environment for the catalytic metal cluster is used in calculations. The probable protonation sites in the cluster and roles of the proton/water transfer channels are discussed in light of the computational results.