Abstract
The electron transfer from the oxygen-evolving Mn(4)CaO(5) cluster to the electron acceptor D1-Tyr161 (TyrZ) is a prerequisite for water oxidation and O(2) 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 S(0) to S(1) 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 S(1) to S(2) 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 S(2) conformation with Mn4(IV) over the formation of the closed-cubane S(2) conformation with Mn1(IV). In the S(0) to S(1) and S(1) to S(2) 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.