Protonation structure of the closed-cubane conformation of the O(2)-evolving complex in photosystem II

In photosystem II (PSII), one-electron oxidation of the most stable state of the oxygen-evolving Mn(4)CaO(5) cluster (S(1)) leads to the S(2) state formation, Mn1(III)Mn2(IV)Mn3(IV)Mn4(IV) (open-cubane S(2)) or Mn1(IV)Mn2(IV)Mn3(IV)Mn4(III) (closed-cubane S(2)). In electron paramagnetic resonance (EPR) spectroscopy, the g = 4.1 signal is not observed in cyanobacterial PSII but in plant PSII, whereas the g = 4.8 signal is observed in cyanobacterial PSII and extrinsic-subunit-depleted plant PSII. Here, we investigated the closed-cubane S(2) conformation, a candidate for a higher spin configuration that accounts for g > 4.1 EPR signal, considering all pairwise exchange couplings in the PSII protein environment (i.e. instead of considering only a single exchange coupling between the [Mn(3)(CaO(4))] cubane region and the dangling Mn4 site). Only when a ligand water molecule that forms an H-bond with D1-Asp61 (W1) is deprotonated at dangling Mn4(IV), the g = 4.1 EPR spectra can be reproduced using the cyanobacterial PSII crystal structure. The closed-cubane S(2) is less stable than the open-cubane S(2) in cyanobacterial PSII, which may explain why the g = 4.1 EPR signal is absent in cyanobacterial PSII.