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

The Mn 4 CaO 5 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, S 3 , forming Mn 4 CaO 6 . 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 S 2 to S 3 transition, resulting in O •- at W1 and protonated D1-Asp61. During the process of Mn 4 CaO 6 formation, O •- , rather than H 2 O 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 S 3 , 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 S 2 valence state) to Mn1(IV)Mn2(IV)Mn3(IV)Mn4(III) (equivalent to the closed-cubane S 2 valence state) occurs. These findings provide energetic insights into the deprotonation and structural conversion events required for the Mn 4 CaO 6 formation.