Quinones and tyrosines in the long-range donor-acceptor side interactions in photosystem II: Implications for proton-coupled electron transfer

It has long been known that certain changes in the acceptor (reductive) side of the Photosystem II (PSII) reaction center lead to alterations on the donor (oxidative) side. However, the nature of this long-range interaction remains unclear. In PSII, the proton-coupled electron transfer is carried out by plastoquinones, Q A and Q B , on the acceptor side and by the tyrosine residues, D1-Tyr161 (Tyr Z ) and D2-Tyr160 (Tyr D ), on the donor side. All four redox components share a similar head-group structure, are symmetrically located on the D1 and D2 core proteins and interact with histidine residues that serve as H-bonding partners. These histidine residues are D1-His215 (His B ), D1-His190 (His Z ), D2-His214 (His A ) and D2-His189 (His D ) respectively. The corresponding histidines of the Q B /Tyr Z pair and Q A /Tyr D pair are bound by the same transmembrane α-helix D of the corresponding D1 or D2 protein ~35 Å apart. It is hypothesized that changes in H-bonding accompanying reduction of acceptor side components are propagated along α-helix D, inducing corresponding alterations in the H-bonding of the donor side components, thereby facilitating their oxidation, and vice versa. Thus, the specific H-bond environment of the single electron acceptor Q A determines the oxidized state of Tyr D in active PSII. When Tyr D is oxidized, Q A is more favorably poised to accept an electron and to transfer it to Q B . On the other hand, the proton-coupled electron reduction and exchange of Q B governs Tyr Z oxidation and reduction during PSII turnover. The structural, functional and evolutionary implications of the proposed mechanism of long-range interactions in PSII are discussed in the context of possible computational and experimental methodologies that can be employed to test this hypothesis.