Abstract
Photosystem II (PSII) is a multisubunit pigment–protein complex that uses light-induced charge separation to power oxygenic photosynthesis. Its reaction center chromophores, where the charge transfer cascade is initiated, are arranged symmetrically along the D1 and D2 core polypeptides and comprise four chlorophyll (PD1, PD2, ChlD1, ChlD2) and two pheophytin molecules (PheoD1 and PheoD2). Evolution favored productive electron transfer only via the D1 branch, with the precise nature of primary excitation and the factors that control asymmetric charge transfer remaining under investigation. Here we present a detailed atomistic description for both. We combine large-scale simulations of membrane-embedded PSII with high-level quantum-mechanics/molecular-mechanics (QM/MM) calculations of individual and coupled reaction center chromophores to describe reaction center excited states. We employ both range-separated time-dependent density functional theory and the recently developed domain based local pair natural orbital (DLPNO) implementation of the similarity transformed equation of motion coupled cluster theory with single and double excitations (STEOM-CCSD), the first coupled cluster QM/MM calculations of the reaction center. We find that the protein matrix is exclusively responsible for both transverse (chlorophylls versus pheophytins) and lateral (D1 versus D2 branch) excitation asymmetry, making ChlD1 the chromophore with the lowest site energy. Multipigment calculations show that the protein matrix renders the ChlD1 → PheoD1 charge-transfer the lowest energy excitation globally within the reaction center, lower than any pigment-centered local excitation. Remarkably, no low-energy charge transfer states are located within the “special pair” PD1–PD2, which is therefore excluded as the site of initial charge separation in PSII. Finally, molecular dynamics simulations suggest that modulation of the electrostatic environment due to protein conformational flexibility enables direct excitation of low-lying charge transfer states by far-red light.
Highlights
Photosystem II (PSII) is a dimeric multisubunit protein−pigment complex responsible for the light-driven oxidation of water into molecular oxygen and for the supply of reducing equivalents in oxygenic photosynthesis.[1−7] Excitation-induced charge separation and the early steps of the electron transfer cascade take place within a cluster of six chlorin molecules known as the reaction center (RC)
We presented large scale MM−MD and QM/MM results on a complete membrane embedded PSII monomer, focusing on excitation energies of single and paired reaction center chromophores
Our results demonstrate explicitly that the excitation asymmetry in the reaction center of PSII is not an intrinsic property of RC chromophores and does not originate from their distinct geometric distortion or coordination
Summary
Pigment complex responsible for the light-driven oxidation of water into molecular oxygen and for the supply of reducing equivalents in oxygenic photosynthesis.[1−7] Excitation-induced charge separation and the early steps of the electron transfer cascade take place within a cluster of six chlorin molecules known as the reaction center (RC). Following excitation and charge separation within the RC chromophores, the radical anion is localized within 0.3−3. With an estimated reduction potential of 1.1−1.3 V, P680+ is able to drive the oxidation of water at the oxygen-evolving complex (OEC) via a redox active tyrosine residue (Tyr[161] or YZ) that interfaces the two sites. A distinctive feature of PSII is the utilization of the D1 branch, which harbors the OEC, for electron transfer following productive charge separation. On the acceptor side the negative charge proceeds from PheoD1 to plastoquinone QA and to the terminal mobile electron acceptor plastoquinone QB.[16]
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