A Simulation of the Isotropic EXAFS Spectra for the S2 and S3 Structures of the Oxygen Evolving Complex in Photosystem II

Most of the main features of water oxidation in photosystem II are now quite well understood, including the mechanism for O-O bond formation. For the intermediate S2 and S3 structures there is also nearly complete agreement between theory and experiments. Given the present high degree of consensus between theory and spectroscopic experiments for these structures, it is of high interest to go back to previous suggestions concerning what happens in the S2 to S3 transition. Analysis of EXAFS experiments have indicated relatively large structural changes in this transition, with changes of distances sometimes larger than 0.3 Å and a change of topology. In contrast, our previous DFT(B3LYP) calculations on a cluster model showed very small changes, less than 0.1 Å Siegbahn, P.E.M. Biochim. Biophys. Acta 2013, 1827, 1003-1019. The main purpose of the present study was therefore to investigate whether the DFT structures are consistent with the EXAFS spectra for both the S2 and S3 states, or if there are differences that suggest significant structural discrepancies. The present EXAFS refinement of the DFT structures now indicates that the DFT structures are topologically correct but that one Mn-Mn distance should increase by +0.13 Å while another one should decrease by -0.09 Å during the S2 to S3 transition, in better agreement with the EXAFS interpretations, and fully consistent with normal errors of DFT(B3LYP). Our results highlight the fact that it is often possible to fit several different structures to the same EXAFS spectrum, a general problem noted before.