Triplet Delocalization over the Reaction Center Chlorophylls in Photosystem II

Abstract

The triplet state of chlorophyll formed by charge recombination in photosystem II (PSII) is a precursor of harmful singlet oxygen. Although main localization of the triplet state on the monomeric chlorophyll, ChlD1, at cryogenic temperatures has been suggested, how the triplet state is delocalized on other chlorophylls remains unclear. Here, we investigated the distribution of the triplet state of chlorophyll in PSII using light-induced Fourier transform infrared (FTIR) difference spectroscopy. Measurements of triplet-minus-singlet FTIR difference spectra with PSII core complexes from cyanobacterial mutants, D1-V157H, D2-V156H, D2-H197A, and D1-H198A, in which the interactions of the 131-keto CO groups of the reaction center chlorophylls, PD1, PD2, ChlD1, and ChlD2, respectively, were perturbed, identified the 131-keto CO bands of the individual chlorophylls and showed that the triplet state is delocalized over all of these chlorophylls. It is suggested that the triplet delocalization plays important roles in the photoprotection and photodamage mechanisms in PSII.

Triplet states in the reaction center of Photosystem II

“…Understanding this phenomenon of triplet delocalization among RC pigments is crucial for comprehending the mechanisms of photo-quenching and photoprotection in PSII. 51,87 Moreover, obtaining accurate estimates of the triplet energy gaps among individual pigments is necessary to determine the actual rates of photo-quenching. To address this, we conducted further QM/MM geometry optimizations of the individual pigments (Chl D1 , Chl D2 , P D1 , and P D2 ) in their singlet and triplet states, enabling us to estimate the adiabatic T 1 –S 0 energy gaps for each chlorophyll.…”

“…Thus, non-radiative energy dissipation involving multiple RC pigments might be a possibility in the closed RC, in line with arguments regarding triplet delocalization pathways discussed in recent FTIR studies. 87 When Q A is doubly reduced as Q A H 2 , the Pheo D1 − anion is expected to be more stable in the absence of a negative charge in its vicinity. 25,45,46,130 This can stabilize 1 [P 680 + Pheo D1 − ] and a subsequent spin inversion to 3 [P 680 + Pheo D1 − ] may again lead to more centers favoring the triplet route as opposed to a direct charge recombination to the singlet state.…”

“…12,24,85,86 However, a coherent description of excited and ground triplet states is lacking. The excitation profiles of all RC pigments in their triplet states are important elements for establishing possible routes of triplet delocalization 87,88 and triplet–triplet energy transfer (T-TET) onto other pigments within the PSII core complex. 89…”

Absorption changes in Photosystem II in the Soret band region upon the formation of the chlorophyll cation radical [P D1 P D2 ] +

“…Finally, we have repeated the experiment in the D2/H197A mutant done in Synechocystis PCC 6803 (Hayase et al 2023). In this mutant, the histidine axial ligand of P D2 has been replaced by an alanine unable to bind to the Mg 2+ of P D2 (see Fig.…”

“…In this mutant, the histidine axial ligand of P D2 has been replaced by an alanine unable to bind to the Mg 2+ of P D2 (see Fig. 1) and it has been already studied (Diner et al 2001, Hayase et al 2023). Panel A in Fig.…”