Mechanism of Oxygen Evolution and Mn₄CaO₅ Cluster Restoration in the Natural Water-Oxidizing Catalyst

Water oxidation occurring in the first steps of natural oxygenic photosynthesis is catalyzed by the pigment/protein complex Photosystem II. This process takes place on the Mn₄Ca cluster located in the core of Photosystem II and proceeds along the five steps (S₀-S₄) of the so-called Kok-Joliot cycle until the release of molecular oxygen. The catalytic cycle can therefore be started afresh through insertion of a new water molecule. Here, combining quantum mechanics/molecular mechanics simulations and minimum energy path calculations, we characterized on different spin surfaces the events occurring in the last sector of the catalytic cycle from structural, electronic, and thermodynamic points of view. We found that the process of oxygen evolution and water insertion can be described well by a two-step mechanism, with oxygen release being the rate-limiting step of the process. Moreover, our results allow us to identify the upcoming water molecule required to regenerate the initial structure of the Mn₄Ca cluster in the S₀ state. The insertion of the water molecule was found to be coupled with the transfer of a proton to a neighboring hydroxide ion, thus resulting in the reconstitution of the most widely accepted model of the S₀ state.