Electronic structure of the Mn4OxCa cluster in the S0 and S2 states of the oxygen-evolving complex of photosystem II based on pulse 55Mn-ENDOR and EPR Spectroscopy

The heart of the oxygen-evolving complex (OEC) of photosystem II is a Mn4OxCa cluster that cycles through five different oxidation states (S-0 to S-4) during the light-driven water-splitting reaction cycle. In this study we interpret the recently obtained Mn-55 hyperfine coupling constants of the S-0 and S-2 states of the OEC [Kulik et al. J. Am. Chem. Soc. 2005, 127, 2392-2393] on the basis of Y-shaped spin-coupling schemes with up to four nonzero exchange coupling constants, J. This analysis rules out the presence of one or more Mn(II) ions in S-0 in methanol (3%) containing samples and thereby establishes that the oxidation states of the manganese ions in S-0 and S-2 are, at 4 K, Mn-4(III, III, III, IV) and Mn-4(III, IV, IV, IV), respectively. By applying a structure filter that is based on the recently reported single-crystal EXAFS data on the Mn4OxCa cluster [Yano et al. Science 2006, 314, 821-825] we (i) show that this new structural model is fully consistent with EPR and Mn-55-ENDOR data, (ii) assign the Mn oxidation states to the individual Mn ions, and (iii) propose that the known shortening of one 2.85 angstrom Mn-Mn distance in S-0 to 2.75 angstrom in S-1 [Robblee et al. J. Am. Chem. Soc. 2002, 124, 7459-7471] corresponds to a deprotonation of a mu-hydroxo bridge between Mn-A and Mn-B, i.e., between the outer Mn and its neighboring Mn of the mu(3)-oxo bridged moiety of the cluster. We summarize our results in a molecular model for the S-0 -> S-1 and S-1 -> S-2 transitions.