Electron-Transfer Route in the Early Oxidation States of the Mn4CaO5 Cluster in Photosystem II

The electron transfer from the oxygen-evolving Mn4CaO5 cluster to the electron acceptor D1-Tyr161 (TyrZ) is a prerequisite for water oxidation and O2 evolution. Here, we analyzed the electronic coupling in the rate-limiting electron-transfer transitions using a combined quantum mechanical/molecular mechanical/polarizable continuum model approach. In the S0 to S1 transition, the electronic coupling between the electron-donor Mn3­(III) and TyrZ is small (2 meV). In contrast, the electronic coupling between the dangling Mn4­(III) and TyrZ is significantly large (172 meV), which suggests that the electron transfer proceeds from Mn3­(III) to TyrZ via Mn4­(III). In the S1 to S2 transition, the electronic coupling between Mn4­(III) and TyrZ is also larger (124 meV) than that between Mn1­(III) and TyrZ (1 meV), which favors the formation of the open-cubane S2 conformation with Mn4­(IV) over the formation of the closed-cubane S2 conformation with Mn1­(IV). In the S0 to S1 and S1 to S2 transitions, the Mn4 d-orbital and the TyrZ π-orbital are hybridized via D1-Asp170, which suggests that D1-Asp170 commonly provides a dominant electron-transfer route.