Theoretical Study of the EPR Spectrum of the STyrZ Metalloradical Intermediate State of the O-evolving Complex of Photosystem II

The intermediates trapped during the transitions between the consecutive S-states of the oxygen-evolving complex (OEC) of photosystem II (PSII) contain the free radical TyrZ interacting magnetically with the Mn-cluster (MnCa). In this paper, we present a theoretical study of the EPR spectrum of the STyrZ metalloradical intermediate state, which has been recently detected in MeOH-containing PSII preparations. For this analysis, we use two different approximations: the first, simpler one, is the point-dipole approach, where the two interacting spins are the S = 1/2 of TyrZ and the ground spin state of S = 3 of the OEC being in the S state. The second approximation is based on previous proposals indicating that the ground spin state (S  = 3) of the S state arises from an antiferromagnetic exchange coupling between the S = 9/2 of the Mn(IV)CaO and the S = 3/2 of the external Mn(IV) of the OEC. Under the above assumption, the second approximation involves three interacting spins, denoted S (Mn(IV)Ca) = 9/2, S (Mn(IV)) = 3/2 and S (TyrZ) = 1/2. Accordingly, the tyrosine radical is exposed to dipolar interactions with both fragments of the OEC, while an antiferromagnetic exchange coupling within the "3 + 1" structural motif of the OEC is also considered. By application of the first-point-dipole approach, the inter-spin distance that simulates the experimental spectrum is not consistent with the theoretical models that were recently reported for the OEC in the S state. Instead, the recent models are consistent with the results of the analysis that is performed by using the second, more detailed, approach.