Theoretical reflections on the structural polymorphism of the oxygen-evolving complex in the S state and the correlations to substrate water exchange and water oxidation mechanism in photosynthesis.

The structural polymorphism of the oxygen-evolving complex is of great significance to photosynthetic water oxidation. Employing density functional theory calculations, we have made further advisement on the interconversion mechanism of O5 transfer in the S state, mainly focusing on the potentiality of multi-state reactivity and spin transitions. Then, O5 protonation is proven impossible in S for irreversibility of the interconversion, which serves as an auxiliary judgment for the protonation state of O5 in S. Besides, the structural polymorphism could also be archived by alternative mechanisms involving Mn3 ligand exchange, one of which with Mn3(III) makes sense to substrate water exchange in S, although being irresponsible for the derivations of the observed EPR signals. During the water exchange, high-spin states would prevail to facilitate electron transfer between the ferromagnetically coupled Mn centers. In addition, water exchange in S could account for the closed-cubane structure as the initial form entering S at cryogenic temperatures. With regard to water oxidation, the structural flexibility and variability in both S and S guarantee smooth W2-O5 coupling in S, according to the substrate assignments from water exchange kinetics. Within this theoretical framework, the new XFEL findings on S-S can be readily rationalized. Finally, an alternative mechanistic scenario for OO bond formation with ·OH radical near O4 is presented, followed by water binding to the pivot Mn4(III) from O4 side during S-S. This may diversify the substrate sources combined with the Ca channel in water delivery for the forthcoming S-cycle.