Identification of the protonation and oxidation states of the oxygen-evolving complex in the low-dose X-ray crystal structure of photosystem II

In photosystem II (PSII), the O3 and O4 sites of the Mn4CaO5 cluster form hydrogen bonds with D1-His337 and a water molecule (W539), respectively. The low-dose X-ray structure shows that these hydrogen bond distances differ between the two homogeneous monomer units (A and B) [Tanaka et al., J. Am Chem. Soc. 2017, 139, 1718]. We investigated the origin of the differences using a quantum mechanical/molecular mechanical (QM/MM) approach. QM/MM calculations show that the short O4-O-W539 hydrogen bond (similar to 2.5 angstrom) of the B monomer is reproduced when O4 is protonated in the S-1 state. The short O3-N epsilon(His337) hydrogen bond of the A monomer is due to the formation of a low-barrier hydrogen bond between O3 and doubly-protonated D1-His337 in the overreduced states (S-1 or S-2). It seems plausible that the oxidation state differs between the two monomer units in the crystal.

Automated summary

The Mn4CaO5 cluster in photosystem II forms hydrogen bonds with D1-His337 and a water molecule. The hydrogen bond distances differ between the two monomer units and can be attributed to protonation and overreduction states.