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 pi-orbital are hybridized via D1-Asp170, which suggests that D1-Asp170 commonly provides a dominant electron-transfer route.

Automated summary

Using a combined quantum mechanical/molecular mechanical/polarizable continuum model approach, we investigated the electronic coupling in the electron-transfer process from the oxygen-evolving Mn4CaO5 cluster to the electron acceptor D1-Tyr161 (TyrZ). Our results showed that the electron transfer occurs from Mn3(III) to TyrZ via Mn4(III) in the S0 to S1 transition, and the formation of the open-cubane S2 conformation with Mn4(IV) is favored over the closed-cubane S2 conformation with Mn1(IV) in the S1 to S2 transition. Additionally, D1-Asp170 was found to play a crucial role as a dominant electron-transfer route.