Triplet States in the Reaction Center of Oxygenic Photosynthesis

Photosystem II (PSII), the first functional protein-pigment complex in the light-driven electron transfer chain of photosynthesis, catalyzes the oxidation of water into molecular oxygen and the reduction of plastoquinone (PQB). The reaction center (RC) of PSII is the site of the primary charge separation upon photoexcitation, forming initially the [ChlD1+PheoD1-] radical pair (RP) [1]. When the forward electron transfer from PheoD1 to the initial acceptor plastoquinone PQA is blocked or delayed, a charge recombination and spin dephasing can lead to the formation of triplet states in the RC. These triplet states can produce chemically active singlet oxygen which can lead to photodamage and photoinhibition. They also serve as important probes to investigate the electronic structure and chemical environment of the RC chromophores. EPR/ENDOR and other spectroscopic studies suggest that the ‘primary donor’ triplet is located on an individual accessory chlorophyll (ChlD1 or ChlD2) [2], however the precise nature or location of this triplet state remains unclear. In this work we characterize all possible triplet states that can be formed at the PSII-RC. We employ multi-scale modelling approaches based on quantum-mechanics/molecular-mechanics (QM/MM) calculations, combined with range-separated time-dependent density functional theory (TDA-TDDFT) methods to identify all low-lying triplet excited states at the RC. In addition, we compute zero-field splitting parameters and hyperfine coupling constants to enable comparisons with experiment. Our results show that the lowest energy triplet is localised on a monomeric chlorophyll, in agreement with experimental interpretations. We further extend our methodology on pigment-pairs to include coupled interactions that may lead to radical-pair charge recombination, and propose a plausible step-by-step pathway that leads to formation of the observable triplet state. This work provides a basis for the atomic level understanding of secondary electron transfer pathways involving photosynthetic pigments and photo-protection mechanisms when the PSII-RC is exposed to excess light conditions