Water oxidation in photosynthetic organisms occurs through the five intermediate steps S_0–S_4 of the Kok cycle in the oxygen evolving complex of photosystem II (PSII). Along the catalytic cycle, four electrons are subsequently removed from the Mn_4CaO_5 core by the nearby tyrosine Tyr-Z, which is in turn oxidized by the chlorophyll special pair P680, the photo-induced primary donor in PSII. Recently, two Mn_4CaO_5 conformations, consistent with the S_2 state (namely, S_2~Aand S_2~B models) were suggested to exist, perhaps playing a different role within the S_2-to-S_3 transition. Here we report multiscale ab initio density functional theory plus U simulations revealing that upon such oxidation the relative thermodynamic stability of the two previously proposed geometries is reversed, the S_2~B state becoming the leading conformation. In this latter state a proton coupled electron transfer is spontaneously observed at ～100 fs at room temperature dynamics. Upon oxidation, the Mn cluster, which is tightly electronically coupled along dynamics to the Tyr-Z tyrosyl group, releases a proton from the nearby W1 water molecule to the close Asp-61 on the femtosecond timescale, thus undergoing a conformational transition increasing the available space for the subsequent coordination of an additional water molecule. The results can help to rationalize previous spectroscopic experiments and confirm, for the first time to our knowledge, that the water-splitting reaction has to proceed through the S_2~B conformation,providing the basis for a structural model of the S_3 state.
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