Pivotal role of the redox-active tyrosine in driving the water splitting catalyzed by photosystem II

Photosynthetic water oxidation is catalyzed by the Mn₄Ca cluster in photosystem II (PSII). The nearby redox-active tyrosine (Y_Z) serves as a direct electron acceptor of the Mn₄Ca cluster and it forms a low-barrier H-bond (LBHB) with a neighboring histidine residue (D1-His190). Experimental evidence indicates that Y_Z oxidation triggers changes in the hydrogen bonding network that precede proton abstraction from the Mn₄Ca cluster. In order to characterize such changes, we compare ab initio molecular dynamics simulations of different states of the catalytic cycle of PSII with dynamics of isolated tyrosine models (namely, p-cresol) in different oxidation states. The systematic comparison of the H-bond networks in different simulated systems suggests that the Y_Z oxidation leads to a water hydration pattern which is more similar to that of the neutral p-cresol rather than that of the p-cresol anion. Our simulations also reveal the twofold nature of the interactions between Y_Z and the Mn₄Ca cluster. Firstly, the Y_Z oxidation triggers rapid structural changes of the H-bond pattern in the proximity of the cluster which have been observed to propagate on the ps time scale on the Ca²⁺ hydration shell up to other water molecules in the proximity of the cluster. Secondly, it is clear that Y_Z interacts with the Mn₄Ca cluster also through Coulombic interactions mediated by CP43-Arg357 through the remaining positive charge of the pair. Our results are able to identify, for the first time, the structural rearrangements guided by the oxidation of Y_Z necessary for the evolution of the water splitting reaction in PSII. Based on these findings, we propose a mechanism of structural changes which is functional towards the progression of the catalytic cycle in PSII.