Microsolvation of the Redox-Active Tyrosine-D in Photosystem II: Correlation of Energetics with EPR Spectroscopy and Oxidation-Induced Proton Transfer

Photosystem II (PSII) of oxygenic photosynthesis captures sunlight to drive the catalytic oxidation of water and the reduction of plastoquinone. Among the several redox-active cofactors that participate in intricate electron transfer pathways there are two tyrosine residues, YZ and YD. They are situated in symmetry-related electron transfer branches but have different environments and play distinct roles. YZ is the immediate oxidant of the oxygen-evolving Mn4CaO5 cluster, whereas YD serves regulatory and protective functions. The protonation states and hydrogen-bond network in the environment of YD remain debated, while the role of microsolvation in stabilizing different redox states of YD and facilitating oxidation or mediating deprotonation, as well the fate of the phenolic proton, is unclear. Here we present detailed structural models of YD and its environment using large-scale quantum mechanical models and all-atom molecular dynamics of a complete PSII monomer. The energetics of water distribution wit...