Charge transfer from the carotenoid can quench chlorophyll excitation in antenna complexes of plants

Cupellini, Lorenzo; Calvani, Dario; Jacquemin, Denis; Mennucci, Benedetta

doi:10.1038/s41467-020-14488-6

Cited by 100 publications

(113 citation statements)

References 60 publications

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“…1 and thererfore represents a complete toolbox. Furthermore, a good overall agreement to another widely used diabatization procedure, namely the multi-state FED-FCD approach [25,75,76,77], has been found, which underlines the usefulness of both approaches.…”

Section: Discussionsupporting

confidence: 56%

Electronic couplings for photo-induced processes from subsystem time-dependent density-functional theory: The role of the diabatization

Tölle

Cupellini

Mennucci

et al. 2020

The Journal of Chemical Physics

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Subsystem time-dependent density-functional theory (sTDDFT) making use of approximate non-additive kinetic energy (NAKE) functionals is known to be capable of describing excitation energy transfer (EET) processes in a variety of applications.Here we show that sTDDFT, especially when combined with projection-based embedding (PbE), can be employed for the entire range of photo-induced electronic couplings essential for modeling photophysical properties of complex chemical and biological systems, and therefore represents a complete toolbox for this class of problems. This means it is capable to capture the interaction/coupling associated with local-and charge-transfer (CT) excitons. However, this requires the choice of a reasonable diabatic basis. We therefore propose different diabatization strategies of the virtual orbital space in PbE-sTDDFT and show how CT excitations can be included in sTDDFT using NAKE functionals via a phenomenological approach.Finally, these electronic couplings are compared to couplings from a multistate fragment excitation difference (FED)-fragment charge difference (FCD) diabatization procedure. We show that both procedures, multistate FED-FCD and sTDDFT (with the right diabatization procedure chosen), lead to an overall good agreement for the electronic couplings, despite differences in their general diabatization strategy. We conclude that the entire range of photo-induced electronic couplings can be obtained using sTDDFT (with the right diabatization procedure chosen) in a black-box manner.

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Section: Discussionsupporting

confidence: 56%

Electronic couplings for photo-induced processes from subsystem time-dependent density-functional theory: The role of the diabatization

Tölle

Cupellini

Mennucci

et al. 2020

The Journal of Chemical Physics

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“…Finally, we recall that some of us have recently proposed that quenching could proceed through charge-transfer states in trimeric LHCII [73]. The charge-transfer mechanism was predicted to be extremely selective and to occur only in the L1 site of LHCII, because both the electronic coupling and the driving force are sensitive to small variations in the Car-Chl distances and orientation and to different electric fields in the two sites.…”

Section: Discussionmentioning

confidence: 94%

The energy transfer model of nonphotochemical quenching: Lessons from the minor CP29 antenna complex of plants

Lapillo

Cignoni

Cupellini

et al. 2020

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Antenna complexes in photosystems of plants and green algae are able to switch between a light-harvesting unquenched conformation and a quenched conformation so to avoid photodamage. When the switch is activated, nonphotochemical quenching (NPQ) mechanisms take place for an efficient deactivation of excess excitation energy. The molecular details of these mechanisms have not been fully clarified but different hypotheses have been proposed. Among them, a popular one involves excitation energy transfer (EET) from the singlet excited Chls to the lowest singlet state (S 1) of carotenoids. In this work, we combine such model with µs-long molecular dynamics simulations of the CP29 minor antenna complex to investigate how conformational fluctuations affect the electronic couplings and the final EET quenching. The computational framework is applied to both CP29 embedding violaxanthin and zeaxantin in its L2 site. Our results demonstrate that the EET model is rather insensitive to physically reasonable variations in single chlorophyll-carotenoid couplings, and that very large conformational changes would be needed to see the large variation of the complex lifetime expected in the switch from light-harvesting to quenched state. We show, however, that a major role in regulating the EET quenching is played by the S 1 energy of the carotenoid, in line with very recent spectroscopy experiments.

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“…Full Time-Dependent Density Functional Theory (TD-DFT), i.e., without the Tamm–Dancoff approximation, was used to compute the excited state properties using the range-separated ωB97X-D3(BJ) 146 − 148 functional along with the Def2-TZVP basis set. The choice of functional was guided by its highly successful application in related studies of biological chromophores 149 and its established superior performance for the treatment of charge-transfer states with TD-DFT. 150 The appropriateness of the functional is additionally confirmed in the present work via direct comparisons with coupled cluster theory.…”

Section: Methodsmentioning

confidence: 99%

Protein Matrix Control of Reaction Center Excitation in Photosystem II

2020

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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 (P D1 , P D2 , Chl D1 , Chl D2 ) and two pheophytin molecules (Pheo D1 and Pheo D2 ). 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 Chl D1 the chromophore with the lowest site energy. Multipigment calculations show that the protein matrix renders the Chl D1 → Pheo D1 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” P D1 –P D2 , 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.

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Charge transfer from the carotenoid can quench chlorophyll excitation in antenna complexes of plants

Cited by 100 publications

References 60 publications

Electronic couplings for photo-induced processes from subsystem time-dependent density-functional theory: The role of the diabatization

Electronic couplings for photo-induced processes from subsystem time-dependent density-functional theory: The role of the diabatization

The energy transfer model of nonphotochemical quenching: Lessons from the minor CP29 antenna complex of plants

Protein Matrix Control of Reaction Center Excitation in Photosystem II

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