Influence of the Ca2Â + ion on the Mn4Ca conformation and the H-bond network arrangement in Photosystem II

In the crystal structure of Photosystem II (PSII) analyzed at a resolution of 1.9 Å, most of the bond lengths between Mn and O atoms in the oxygen-evolving Mn4Ca cluster are 1.8-2.1 Å. On the other hand, the Mn1O5 bond in the Mn3CaO4 cubane region of the Mn4Ca cluster is significantly elongated to 2.6 Å. Using a quantum mechanical/molecular mechanical approach, we investigated factors that are responsible for distortion of the Mn3CaO4 cubane. Removal of Ca led to shortening the Mn1O5 bond by 0.2 Å; however, Mn1O5 remained significantly elongated, at > 2.5 Å. Conversely, removal of Mn4 significantly shortens the Mn1O5 distance by 0.5 Å to 2.2 Å, resulting in a more symmetric cubane shape. These results suggest that Mn4, not Ca, is predominantly responsible for distortion of the Mn3CaO4 cubane. It was not the Ca component that was responsible for the existence of the two S2 conformers but two different Mn oxidation states (Mn1, Mn2, Mn3, M4) = (III, IV, IV, IV) and (IV, IV, IV, III); they were interconvertible by translocation of the O5 atom along the Mn1-O5-Mn4 axis. Depletion of Ca resulted in rearrangement of the H-bond network near TyrZ, which proceeds via a chloride ion (Cl-1 pathway). This may explain why Ca depletion inhibits the S2 to S3 transition, the same process that can also be inhibited by Cl− depletion.