Origin of Low-Lying Red States in the Lhca4 Light-Harvesting Complex of Photosystem I

Vladislav Sláma; Lorenzo Cupellini; Vincenzo Mascoli; Nicoletta Liguori; Roberta Croce; Benedetta Mennucci

doi:10.1021/acs.jpclett.3c02091

Origin of Low-Lying Red States in the Lhca4 Light-Harvesting Complex of Photosystem I

Vladislav Sláma^*
, Lorenzo Cupellini^*
, Vincenzo Mascoli
, Nicoletta Liguori
, Roberta Croce
, Benedetta Mennucci

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

The antenna complexes of Photosystem I present low-lying states visible as red-shifted and broadened absorption and fluorescence bands. Among these, Lhca4 has the most evident features of these “red” states, with a fluorescence band shifted by more than 25 nm from typical LHC emission. This signal arises from a mixing of exciton and charge-transfer (CT) states within the excitonically coupled a603-a609 chlorophyll (Chl) dimer. Here we combine molecular dynamics, multiscale quantum chemical calculations, and spectral simulations to uncover the molecular mechanism for the formation and tuning of exciton-CT interactions in Lhca4. We show that the coupling between exciton and CT states is extremely sensitive to tiny variations in the Chl dimer arrangement, explaining both the red-shifted bands and the switch between conformations with blue and red emission observed in single-molecule spectroscopy. Finally, we show that mutating the axial ligand of a603 diminishes the exciton-CT coupling, removing any red-state fingerprint.

Original language	English
Pages (from-to)	8345-8352
Number of pages	8
Journal	Journal of Physical Chemistry Letters
Volume	14
Issue number	37
Early online date	13 Sept 2023
DOIs	https://doi.org/10.1021/acs.jpclett.3c02091
Publication status	Published - 21 Sept 2023

Bibliographical note

Funding Information:
V.S., L.C., and B.M. acknowledge funding by the European Research Council (ERC), under the grant ERC-AdG-786714 (LIFETimeS), and V.M., N.L., and R.C. from the Dutch Organization for Scientific research (NWO) via a Top grant to R.C. and a Veni grant to N.L.

Publisher Copyright:
© 2023 The Authors. Published by American Chemical Society.

Funding

V.S., L.C., and B.M. acknowledge funding by the European Research Council (ERC), under the grant ERC-AdG-786714 (LIFETimeS), and V.M., N.L., and R.C. from the Dutch Organization for Scientific research (NWO) via a Top grant to R.C. and a Veni grant to N.L.

Funders	Funder number
European Research Council
Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Horizon 2020 Framework Programme	786714

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title = "Origin of Low-Lying Red States in the Lhca4 Light-Harvesting Complex of Photosystem I",

abstract = "The antenna complexes of Photosystem I present low-lying states visible as red-shifted and broadened absorption and fluorescence bands. Among these, Lhca4 has the most evident features of these “red” states, with a fluorescence band shifted by more than 25 nm from typical LHC emission. This signal arises from a mixing of exciton and charge-transfer (CT) states within the excitonically coupled a603-a609 chlorophyll (Chl) dimer. Here we combine molecular dynamics, multiscale quantum chemical calculations, and spectral simulations to uncover the molecular mechanism for the formation and tuning of exciton-CT interactions in Lhca4. We show that the coupling between exciton and CT states is extremely sensitive to tiny variations in the Chl dimer arrangement, explaining both the red-shifted bands and the switch between conformations with blue and red emission observed in single-molecule spectroscopy. Finally, we show that mutating the axial ligand of a603 diminishes the exciton-CT coupling, removing any red-state fingerprint.",

author = "Vladislav Sl{\'a}ma and Lorenzo Cupellini and Vincenzo Mascoli and Nicoletta Liguori and Roberta Croce and Benedetta Mennucci",

note = "Funding Information: V.S., L.C., and B.M. acknowledge funding by the European Research Council (ERC), under the grant ERC-AdG-786714 (LIFETimeS), and V.M., N.L., and R.C. from the Dutch Organization for Scientific research (NWO) via a Top grant to R.C. and a Veni grant to N.L. Publisher Copyright: {\textcopyright} 2023 The Authors. Published by American Chemical Society.",

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AU - Sláma, Vladislav

AU - Cupellini, Lorenzo

AU - Mascoli, Vincenzo

AU - Liguori, Nicoletta

AU - Croce, Roberta

AU - Mennucci, Benedetta

N1 - Funding Information: V.S., L.C., and B.M. acknowledge funding by the European Research Council (ERC), under the grant ERC-AdG-786714 (LIFETimeS), and V.M., N.L., and R.C. from the Dutch Organization for Scientific research (NWO) via a Top grant to R.C. and a Veni grant to N.L. Publisher Copyright: © 2023 The Authors. Published by American Chemical Society.

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N2 - The antenna complexes of Photosystem I present low-lying states visible as red-shifted and broadened absorption and fluorescence bands. Among these, Lhca4 has the most evident features of these “red” states, with a fluorescence band shifted by more than 25 nm from typical LHC emission. This signal arises from a mixing of exciton and charge-transfer (CT) states within the excitonically coupled a603-a609 chlorophyll (Chl) dimer. Here we combine molecular dynamics, multiscale quantum chemical calculations, and spectral simulations to uncover the molecular mechanism for the formation and tuning of exciton-CT interactions in Lhca4. We show that the coupling between exciton and CT states is extremely sensitive to tiny variations in the Chl dimer arrangement, explaining both the red-shifted bands and the switch between conformations with blue and red emission observed in single-molecule spectroscopy. Finally, we show that mutating the axial ligand of a603 diminishes the exciton-CT coupling, removing any red-state fingerprint.

AB - The antenna complexes of Photosystem I present low-lying states visible as red-shifted and broadened absorption and fluorescence bands. Among these, Lhca4 has the most evident features of these “red” states, with a fluorescence band shifted by more than 25 nm from typical LHC emission. This signal arises from a mixing of exciton and charge-transfer (CT) states within the excitonically coupled a603-a609 chlorophyll (Chl) dimer. Here we combine molecular dynamics, multiscale quantum chemical calculations, and spectral simulations to uncover the molecular mechanism for the formation and tuning of exciton-CT interactions in Lhca4. We show that the coupling between exciton and CT states is extremely sensitive to tiny variations in the Chl dimer arrangement, explaining both the red-shifted bands and the switch between conformations with blue and red emission observed in single-molecule spectroscopy. Finally, we show that mutating the axial ligand of a603 diminishes the exciton-CT coupling, removing any red-state fingerprint.

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Origin of Low-Lying Red States in the Lhca4 Light-Harvesting Complex of Photosystem I

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