Formation of the High-Spin S2 State Related to the Extrinsic Proteins in the Oxygen Evolving Complex of Photosystem II

The high-spin S-2 state was investigated with photosystem II (PSII) from spinach, Thermosynechococcus vulcanus, and Cyanidioschyzon merolae. In extrinsic protein-depleted PSII, high-spin electron paramagnetic resonance (EPR) signals were not detected in either species, whereas all species showed g similar to 5 signals in the presence of a high concentration of Ca2+ instead of the multiline signal. In the intact and PsbP/Qdepleted PSII from spinach, the g = 4.1 EPR signal was detected. These results show that formation of the high-spin S-2 state of the manganese cluster is regulated by the extrinsic proteins through a charge located near the Mn4 atom in the Mn4CaO5 cluster but is independent of the intrinsic proteins. The shift to the g similar to 5 state is caused by tilting of the z-axis in the Mn4 coordinates through hydrogen bonds or external divalent cations. The structural modification may allow insertion of an oxygen atom during the S-2-to-S-3 transition.