Mechanism of proton-coupled quinone reduction in Photosystem II.

Photosystem II uses light to drive water oxidation and plastoquinone (PQ) reduction. PQ reduction involves two PQ cofactors, QA and QB, working in series. QA is a one-electron carrier, whereas QB undergoes sequential reduction and protonation to form QBH2. QBH2 exchanges with PQ from the pool in the membrane. Based on the atomic coordinates of the Photosystem II crystal structure, we analyzed the proton transfer (PT) energetics adopting a quantum mechanical/molecular mechanical approach. The potential-energy profile suggests that the initial PT to QB•- occurs from the protonated, D1-His252 to QB•- via D1-Ser264. The second PT is likely to occur from D1-His215 to QBH- via an H-bond with an energy profile with a single well, resulting in the formation of QBH2 and the D1-His215 anion. The pathway for reprotonation of D1-His215- may involve bicarbonate, D1-Tyr246 and water in the QB site. Formate ligation to Fe2+ did not significantly affect the protonation of reduced QB, suggesting that formate inhibits QBH2 release rather than its formation. The presence of carbonate rather than bicarbonate seems unlikely because the calculations showed that this greatly perturbed the potential of the nonheme iron, stabilizing the Fe3+ state in the presence of QB•-, a situation not encountered experimentally. H-bonding from D1-Tyr246 and D2-Tyr244 to the bicarbonate ligand of the nonheme iron contributes to the stability of the semiquinones. A detailed mechanistic model for QB reduction is presented. [ABSTRACT FROM AUTHOR]