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.