Exploring the Deprotonation Process during Incorporation of a Ligand Water Molecule at the Dangling Mn Site in Photosystem II

The Mn4CaO5 cluster, featuring
four ligand
water molecules (W1 to W4), serves as the water-splitting site in
photosystem II (PSII). X-ray free electron laser (XFEL) structures
exhibit an additional oxygen site (O6) adjacent to the O5 site in
the fourth lowest oxidation state, S3, forming Mn4CaO6. Here, we investigate the mechanism of the second
water ligand molecule at the dangling Mn (W2) as a potential incorporating
species, using a quantum mechanical/molecular mechanical (QM/MM) approach.
Previous QM/MM calculations demonstrated that W1 releases two protons
through a low-barrier H-bond toward D1-Asp61 and subsequently releases
an electron during the S2 to S3 transition,
resulting in O•– at W1 and protonated D1-Asp61.
During the process of Mn4CaO6 formation, O•–, rather than H2O or OH–, best reproduced the O5···O6 distance. Although the
catalytic cluster with O•– at O6 is more
stable than that with O•– at W1 in S3, it does not occur spontaneously due to the significantly
uphill deprotonation process. Assuming O•– at W2 incorporates into the O6 site, an exergonic conversion from
Mn1­(III)­Mn2­(IV)­Mn3­(IV)­Mn4­(IV) (equivalent to the open-cubane S2 valence state) to Mn1­(IV)­Mn2­(IV)­Mn3­(IV)­Mn4­(III) (equivalent
to the closed-cubane S2 valence state) occurs. These findings
provide energetic insights into the deprotonation and structural conversion
events required for the Mn4CaO6 formation.