Hey ho, where'd the proton go? Final deprotonation of O6 within the S3 state of photosystem II

Abstract

The deprotonation of O6 within the S₃ state marks the final deprotonation event before the formation of oxygen‑oxygen bond interactions and eventual production and release of dioxygen. Gaining a thorough understanding of this event, from the proton acceptors involved, to the exfiltration pathways available, is key in determining the nature of the resulting oxygen species, influencing the mechanism through which the first oxygen‑oxygen bond forms. Computational analysis, using BS-DFT methodologies, showed that proton abstraction by the local Glu189 residue provides consistent evidence against this being a viable mechanistic pathway due to the lack of a stable product structure. In contrast, abstraction via W3 shows an increasingly stable oxo-oxo product state between r[O5O6] = 2.1 Å & 1.9 Å. The resulting oxo-oxo state is stabilised through donation of $\beta$ electron character from O6 to Mn1 and $\alpha$ electron character from O6 to O5. This donation from the O6 lone pair is shown to be a key factor in stabilising the oxo-oxo state, in addition to showing the initiation of first O5-O6 bond.