Proton-mediated photoprotection mechanism in photosystem II

Yu Sugo; Hiroshi Ishikita

doi:10.3389/fpls.2022.934736

Proton-mediated photoprotection mechanism in photosystem II

Front Plant Sci. 2022 Sep 7:13:934736. doi: 10.3389/fpls.2022.934736. eCollection 2022.

Authors

Yu Sugo¹, Hiroshi Ishikita^{1

2}

Affiliations

¹ Department of Applied Chemistry, The University of Tokyo, Tokyo, Japan.
² Research Center for Advanced Science and Technology, The University of Tokyo, Tokyo, Japan.

Abstract

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 O₂ 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 Fe²⁺ 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_AH^⋅ stabilization, increasing the Q_A redox potential and activating a charge-recombination pathway that does not generate the harmful singlet oxygen.

Keywords: D1-Tyr246; QBH2 release/exchange; bicarbonate; formate; low-barrier hydrogen bond (LBHB); photoinhibition; photoprotection; proton-coupled electron transfer (PCET).