Proton-mediated photoprotection mechanism in photosystem II

Abstract

Photo-induced charge separation, which is terminated by electron transfer from the primary quinone QA to the secondary quinone QB, 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 QA⋅– 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 QA⋅–. The migration of the proton from D2-His214 toward QA⋅– stabilizes QA⋅–. 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 QA⋅–/QAH⋅ stabilization, increasing the QA redox potential and activating a charge-recombination pathway that does not generate the harmful singlet oxygen.

Electron Transfer Route between Quinones in Type-II Reaction Centers

“…In contrast, the existence of a corresponding water molecule at the bicarbonate moiety is inhibited by the bulky side-chain of D1-Tyr246 (bicarbonate···D1-Tyr246 = 3.2 Å), which is conserved even in the earliest evolving D1 proteins . The role of the water molecule in superexchange electron tunneling cannot be substituted by D1-Tyr246, because D1-Tyr246 does not form an H-bond with the bicarbonate O site (unless the bidentate to monodentate reorientation of the bicarbonate ligand occurs). As D1-Tyr246 is located in the de -loop region, which is absent in PbRC but crucial to PSII functioning (e.g., photoinhibition or light susceptibility − ), the low H QA–QB value due to the loss of water molecules is a distinct feature of PSII.…”

Lys264 of the D2 Protein Performs a Dual Role in Photosystem II Modifying Assembly and Electron Transfer through the Quinone–Iron Acceptor Complex

“…The Glu in the K264E mutant could, for example, ligate the non-heme iron directly excluding bicarbonate or formate. Given that binding and release of bicarbonate from the NHI has been implicated in a PS II-specific photoprotection mechanism that minimizes the production of 1 O 2 , 22,24,25,55 we investigated the impact of mutating D2-Lys264 on the susceptibility to high-light-induced photodamage, and the capacity of the K264A and K264E mutants to recover after exposure to high light. Impact of Mutations Targeting D2-Lys264 on Photodamage and Repair.…”

“…A non-heme iron (NHI) (Fe 2+ ) is located between Q A and Q B ; however, the NHI is not redox active. , The NHI is coordinated by two histidine ligands from D1 and two from D2. , In all oxygenic photosynthetic organisms, bicarbonate (or HCO 3 – ) additionally provides a bidentate ligand to the NHI. , Depletion of bicarbonate in the presence of formate impairs both forward electron transfer between Q A and Q B and impairs the Q B H 2 /PQ exchange reactions at the Q B -binding site. − The involvement of bicarbonate in regulating forward electron flow on the acceptor side of PS II suggests bicarbonate binding is essential for the process of photoactivation and assembly of the OEC. , Moreover, accumulation of Q A – , which can arise by over-reduction of the electron transport chain in response to environmental stress, leads to dissociation of bicarbonate from the NHI and an increase of ∼55 mV in the potential of the Q A /Q A – redox couple. , Consequently, the back-reaction between Q A – and P680 + is favored over the back-reaction via the excited state of P680 that leads to 1 O 2 formation. Hence bicarbonate binding (and release) may play a role in photoprotection of PS II. ,, …”

“…Hence bicarbonate binding (and release) may play a role in photoprotection of PS II. 22,24,25 Bound bicarbonate is also associated with a hydrogen bond network that is important for the protonation steps associated with the formation of Q B H 2 . 26−29 Bound bicarbonate is stabilized by hydrogen bonds from D1-Tyr246 and D2-Tyr244 (Figure 1).…”

Cryo-EM insight into hydrogen positions and water networks in photosystem II

“…In addition, internal proton shifts mediated by the proton-water network, such as that between Y Z and the nearby D1-His190, are essential ( 18, 19 ). Thus, the protonation state of critical amino acid sidechains, as well as the positions and interactions of water molecules, are important pieces to the puzzle of how PSII orchestrates both water oxidation and PQ reduction ( 20, 21 ).…”