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A TDDFT investigation of the Photosystem II reaction center: Insights into the precursors to charge separation.

ABSTRACT: Photosystem II (PS II) captures solar energy and directs charge separation (CS) across the thylakoid membrane during photosynthesis. The highly oxidizing, charge-separated state generated within its reaction center (RC) drives water oxidation. Spectroscopic studies on PS II RCs are difficult to interpret due to large spectral congestion, necessitating modeling to elucidate key spectral features. Herein, we present results from time-dependent density functional theory (TDDFT) calculations on the largest PS II RC model reported to date. This model explicitly includes six RC chromophores and both the chlorin phytol chains and the amino acid residues <6 Å from the pigments' porphyrin ring centers. Comparing our wild-type model results with calculations on mutant D1-His-198-Ala and D2-His-197-Ala RCs, our simulated absorption-difference spectra reproduce experimentally observed shifts in known chlorophyll absorption bands, demonstrating the predictive capabilities of this model. We find that inclusion of both nearby residues and phytol chains is necessary to reproduce this behavior. Our calculations provide a unique opportunity to observe the molecular orbitals that contribute to the excited states that are precursors to CS. Strikingly, we observe two high oscillator strength, low-lying states, in which molecular orbitals are delocalized over ChlD1 and PheD1 as well as one weaker oscillator strength state with molecular orbitals delocalized over the P chlorophylls. Both these configurations are a match for previously identified exciton-charge transfer states (ChlD1 +PheD1 -)* and (PD2 +PD1 -)*. Our results demonstrate the power of TDDFT as a tool, for studies of natural photosynthesis, or indeed future studies of artificial photosynthetic complexes.

SUBMITTER: Kavanagh MA

PROVIDER: S-EPMC7443915 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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A TDDFT investigation of the Photosystem II reaction center: Insights into the precursors to charge separation.

Kavanagh Maeve A MA Karlsson Joshua K G JKG Colburn Jonathan D JD Barter Laura M C LMC Gould Ian R IR

Proceedings of the National Academy of Sciences of the United States of America 20200803 33

Photosystem II (PS II) captures solar energy and directs charge separation (CS) across the thylakoid membrane during photosynthesis. The highly oxidizing, charge-separated state generated within its reaction center (RC) drives water oxidation. Spectroscopic studies on PS II RCs are difficult to interpret due to large spectral congestion, necessitating modeling to elucidate key spectral features. Herein, we present results from time-dependent density functional theory (TDDFT) calculations on the ...[more]

PMID: 32747579

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Project description: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.

Dataset Information

A TDDFT investigation of the Photosystem II reaction center: Insights into the precursors to charge separation.

Publications

A TDDFT investigation of the Photosystem II reaction center: Insights into the precursors to charge separation.

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