Electron Transfer Mechanism from the Oxygen-Evolving Complex to the Electron-Acceptor Tyrosine during the S2 to S3 Transition in Photosystem II

Abstract

The mechanism of water oxidation catalyzed by Mn₄CaO₅ in photosystem II lacks consensus, particularly regarding proton-coupled electron transfer in the second flash-induced S₂ to S₃ transition. Here, we investigate the electron transfer mechanism during the S₂ to S₃ transition using a quantum mechanical/molecular mechanical/polarizable continuum model approach. The electrostatic interaction with the oxidized redox-active tyrosine, TyrZ, triggers proton release not from a ligand water molecule near chloride (W2) at dangling Mn (Mn4) or a ligand water molecule at Ca²⁺ (W3), but from a ligand water molecule (W1) near D1-Asp61 at Mn4, forming OH^- at Mn-(IV). OH^- formation at Ca²⁺ is significantly less stable than that at Mn4-(IV). Incorporation of the OH^- species into Mn₄CaO₅ induces a valence-state conversion from (III,IV,IV,IV) to (IV,IV,IV,III). Interestingly, subsequent water incorporation from a water channel and restoration of the H-bond network of TyrZ not only elevate the redox potential of TyrZ but also convert the valence state back to (III,IV,IV,IV), facilitating electron transfer to TyrZ. The electronic coupling between Mn1 and TyrZ is 1 to 3 meV in the S₂ to S₃ transition, significantly smaller than those between Mn4 and TyrZ in the S₀ to S₁ (∼170 meV) and S₁ to S₂ (∼120 meV) transitions. This step serves as the rate-limiting step if [Mn-(IV)]₄ is considered to be the relevant state to S₃.

1

Energy profile for reaction intermediates with OH^– at W1 (with respect to H₂O at W1) in the open-cubane S₂ conformation with Mn1­(III)­Mn2­(IV)­Mn3­(IV)­Mn4­(IV). (State 1–1) H₂O at W1 and deprotonated D1-Asp61 in S₂ in the presence of TyrZ-O^• in S₂. (State 1–2) OH^– at W1 and protonated D1-Asp61 in the presence of TyrZ-O^• in S₂. The transferring H⁺ is highlighted in cyan. For each intermediate state, the first digit indicates the figure number, and the second digit indicates the state number.

2

Energy profile for reaction intermediates with OH^– at W2 (with respect to the open-cubane S₂ conformation). (State 2–1) OH^– at W2 in the open-cubane S₂ conformation with Mn1­(III)­Mn2­(IV)­Mn3­(IV)­Mn4­(IV) in the presence of TyrZ-O^•. (State 2–2) OH^– at W2 in the closed-cubane S₂ conformation with Mn1­(IV)­Mn2­(IV)­Mn3­(IV)­Mn4­(III) in the presence of TyrZ-O^•. For each intermediate state, the first digit indicates the figure number, and the second digit indicates the state number.

3

Energy profile for reaction intermediates with OH^– at W3 (with respect to OH^– at W2). (State 3–1) OH^– at W3 in S₂ in the presence of TyrZ-O^•. (State 3–2) OH^– incorporated into the O6 site from W3, forming the O5···O6–H conformation of S₂ in the presence of TyrZ-O^•. (State 3–2’) OH^– incorporated into the O6 site from W3, forming the O5···H–O6 conformation of S₂. (State 3–3) H₂O incorporated into the W3 site from W7, with the O5···O6–H conformation of S₂. (State 3–3′) H₂O incorporated into the W3 site from W7, with the O5···H–O6 conformation of S₂ in the presence of TyrZ-O^•. (State 3–4) O5···O6–H conformation of S₃ with the established H-bond network in the presence of TyrZ–OH. (State 3–4’) O5···H–O6 conformation of S₃ with the established H-bond network in the presence of TyrZ–OH. Blue dotted circles indicate vacant water binding sites. The H atom of incorporated O6 is colored cyan. For each intermediate state, the first digit indicates the figure number, and the second digit indicates the state number.

4

Changes in the H-bond pattern for TyrZ upon incorporation of a water molecule into the W7 site. (a) Before the incorporation of H₂O into the W7 site in the presence of TyrZ-O^• in S₂. (b) After the incorporation of H₂O into the W7 site in the presence of TyrZ-O^• in S₂, resulting in S₃. Dotted lines indicate representative H-bonds. The blue dotted circle indicates the vacant W7 site.

5

Orbitals at the electron donor Mn₄CaO₆ (Mn1) and acceptor TyrZ moieties in the S₂ to S₃ transition. H _Mn1‑TyrZ represents the electronic coupling between Mn1 and TyrZ. (a) O5···O6–H conformation. (b) O5···H–O6 conformation.

6

Summary of the electron-transfer mechanism for the S₂ to S₃ transition investigated in this study, involving the incorporation of OH^– from W3 into the O6 site and the formation of [Mn­(IV)]₄ as S₃. Although the deprotonation of W3 at Ca²⁺ raises energetic questions, electron transfer to TyrZ-O^• from Mn1­(III) occurs upon completion of the H-bond network of TyrZ, assuming that [Mn­(IV)]₄ with OH^– at O6 is the relevant S₃ species. Brackets highlight high-energy intermediate states.