Proton-mediated photoprotection mechanism in photosystem II

Photo-induced charge separation, which is terminated by electron transfer from the primary quinone Q(A) to the secondary quinone Q(B), provides the driving force for O(2) evolution in photosystem II (PSII). However, the backward charge recombination using the same electron-transfer pathway leads to the triplet chlorophyll formation, generating harmful singlet-oxygen species. Here, we investigated the molecular mechanism of proton-mediated Q(A)(⋅–) stabilization. Quantum mechanical/molecular mechanical (QM/MM) calculations show that in response to the loss of the bicarbonate ligand, a low-barrier H-bond forms between D2-His214 and Q(A)(⋅–). The migration of the proton from D2-His214 toward Q(A)(⋅–) stabilizes Q(A)(⋅–). The release of the bicarbonate ligand from the binding Fe(2+) site is an energetically uphill process, whereas the bidentate-to-monodentate reorientation is almost isoenergetic. These suggest that the bicarbonate protonation and decomposition may be a basis of the mechanism of photoprotection via Q(A)(⋅–)/Q(A)H(⋅) stabilization, increasing the Q(A) redox potential and activating a charge-recombination pathway that does not generate the harmful singlet oxygen.