The first tyrosyl radical intermediate formed in the S2-S3 transition of photosystem II

The EPR split signals'' represent key intermediates of the S-state cycle where the redox active D1-Tyr161 (Y-Z) has been oxidized by the reaction center of the photosystem II enzyme to its tyrosyl radical form, but the successive oxidation of the Mn4CaO5 cluster has not yet occurred (SiYZ center dot). Here we focus on the S2YZ center dot state, which is formed en route to the final metastable state of the catalyst, the S-3 state, the state which immediately precedes O-O bond formation. Quantum chemical calculations demonstrate that both isomeric forms of the S-2 state, the open and closed cubane isomers, can form states with an oxidized Y-Z center dot residue without prior deprotonation of the Mn4CaO5 cluster. The two forms are expected to lie close in energy and retain the electronic structure and magnetic topology of the corresponding S-2 state of the inorganic core. As expected, tyrosine oxidation results in a proton shift towards His190. Analysis of the electronic rearrangements that occur upon formation of the tyrosyl radical suggests that a likely next step in the catalytic cycle is the deprotonation of a terminal water ligand (W1) of the Mn4CaO5 cluster. Diamagnetic metal ion substitution is used in our calculations to obtain the molecular g-tensor of Y-Z center dot. It is known that the g(x) value is a sensitive probe not only of the extent of the proton shift between the tyrosine-histidine pair, but also of the polarization environment of the tyrosine, especially about the phenolic oxygen. It is shown for PSII that this environment is determined by the Ca2+ ion, which locates two water molecules about the phenoxyl oxygen, indirectly modulating the oxidation potential of Y-Z.