Possible mechanisms of water splitting reaction based on proton and electron release pathways revealed for CaMn4O5 cluster of PSII refined to 1.9 Å X-ray resolution

Recently, Umena et al. have revealed the X‐ray diffraction structure of the CaMn4O5 cluster in the oxygen evolving complex (OEC) of photosystem II (PSII) refined to 1.9 Å resolution. Their X‐ray structure has first elucidated hydrogen‐bonding networks and proton release pathways at OEC of PSII. Here, several working hypotheses (heuristic principles) for water splitting reaction are derived from their X‐ray structure for theoretical modeling. These hypotheses suggest how water can be oxidized at OEC of PSII: namely possible reaction mechanisms for the reaction. To confirm them, we have also performed broken‐symmetry (BS) UB3LYP calculations for active site models based on their XRD structure. The bond lengths of formal Mn(V)O with labile dπ‐pπ bonds are optimized to clarify possible roles of the species that are often introduced as a key intermediate in the catalytic (Kok) cycle for water splitting reaction at OEC of PSII. Location of the transition structure for the oxygen‐oxygen (OO) bond formation is also performed by the energy optimization technique. The natural orbital (NO) analysis of the UB3LYP solutions has been performed to obtain the natural molecular orbitals and their occupation numbers that have been useful for classification of localized d‐electrons, labile chemical bonds and closed‐shell (valence) orbitals. The localized d‐electrons characterized by the NO analysis are the origins for the magnetism revealed by ENDOR and other magnetic experiments. On the other hand, the nature of labile (soft) dπ‐pπ bonds responsible for the OO bond formation has been investigated on the basis of chemical indices such as effective bond order (b), diradical character (y), and spin density (Q) indices that are calculated using the orbital overlap between broken‐symmetry orbitals. These chemical indices have been calculated for the transition structure of the OO bond formation at OEC of PSII. Implications of present computational results are discussed in relation to the derived hypotheses and available accumulated experimental results. © 2011 Wiley Periodicals, Inc. Int J Quantum Chem, 2012