Electronic structure of S₂ state of the oxygen-evolving complex of photosystem II studied by PELDOR

Photosynthetic water splitting is catalyzed by a Mn₄CaO ₅ cluster in photosystem II, whose structure was recently determined at a resolution of 1.9 Å [Umena, Y. et al. 2011, Nature, 473:55-60]. To determine the electronic structure of the Mn₄CaO₅ cluster, pulsed electron-electron double resonance (PELDOR) measurements were performed for the tyrosine residue Y_D and S₂ state signals with non-oriented and oriented photosystem II (PS II) samples. Based on these measurements, the spin density distributions were calculated by comparing with the experimental results. The best fitting parameters were obtained with a model in which Mn1 has a large positive projection, Mn3 has a small positive projection, and Mn2 and Mn4 have negative projections (the numbering of Mni (i = 1-4) is based on the crystal structure at a 1.9 Å resolution), which yielded spin projections of 1.97, - 1.20, 1.19 and - 0.96 for Mn1-4 ions. The results show that the Mn1 ion, which is coordinated by H332, D342 and E189, has a valence of Mn(III) in the S₂ state. The sign of the exchange interactions J₁₃ is positive, and the other signs are negative.