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Sub-100-fs energy transfer in coenzyme NADH is a coherent process assisted by a charge-transfer state

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  • Vishal Kumar Jaiswal

    (Università di Bologna)

  • Daniel Aranda Ruiz

    (Universidad de Valencia)

  • Vasilis Petropoulos

    (Politecnico di Milano)

  • Piotr Kabaciński

    (Politecnico di Milano)

  • Francesco Montorsi

    (Università di Bologna)

  • Lorenzo Uboldi

    (Politecnico di Milano)

  • Simone Ugolini

    (Università di Bologna)

  • Shaul Mukamel

    (University of California)

  • Giulio Cerullo

    (Politecnico di Milano)

  • Marco Garavelli

    (Università di Bologna)

  • Fabrizio Santoro

    (Area della Ricerca del CNR)

  • Artur Nenov

    (Università di Bologna)

Abstract

Excitation energy transfer (EET) is a key photoinduced process in biological chromophoric assemblies. Here we investigate the factors which can drive EET into efficient ultrafast sub-ps regimes. We demonstrate how a coherent transport of electronic population could facilitate this in water solvated NADH coenzyme and uncover the role of an intermediate dark charge-transfer state. High temporal resolution ultrafast optical spectroscopy gives a 54±11 fs time constant for the EET process. Nonadiabatic quantum dynamical simulations computed through the time-evolution of multidimensional wavepackets suggest that the population transfer is mediated by photoexcited molecular vibrations due to strong coupling between the electronic states. The polar aqueous solvent environment leads to the active participation of a dark charge transfer state, accelerating the vibronically coherent EET process in favorably stacked conformers and solvent cavities. Our work demonstrates how the interplay of structural and environmental factors leads to diverse pathways for the EET process in flexible heterodimers and provides general insights relevant for coherent EET processes in stacked multichromophoric aggregates like DNA strands.

Suggested Citation

  • Vishal Kumar Jaiswal & Daniel Aranda Ruiz & Vasilis Petropoulos & Piotr Kabaciński & Francesco Montorsi & Lorenzo Uboldi & Simone Ugolini & Shaul Mukamel & Giulio Cerullo & Marco Garavelli & Fabrizio , 2024. "Sub-100-fs energy transfer in coenzyme NADH is a coherent process assisted by a charge-transfer state," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48871-4
    DOI: 10.1038/s41467-024-48871-4
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    References listed on IDEAS

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    1. Rocío Borrego-Varillas & Artur Nenov & Piotr Kabaciński & Irene Conti & Lucia Ganzer & Aurelio Oriana & Vishal Kumar Jaiswal & Ines Delfino & Oliver Weingart & Cristian Manzoni & Ivan Rivalta & Marco , 2021. "Tracking excited state decay mechanisms of pyrimidine nucleosides in real time," Nature Communications, Nature, vol. 12(1), pages 1-7, December.
    2. Eric A. Arsenault & Yusuke Yoneda & Masakazu Iwai & Krishna K. Niyogi & Graham R. Fleming, 2020. "The role of mixed vibronic Qy-Qx states in green light absorption of light-harvesting complex II," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    3. Elisabetta Collini & Cathy Y. Wong & Krystyna E. Wilk & Paul M. G. Curmi & Paul Brumer & Gregory D. Scholes, 2010. "Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature," Nature, Nature, vol. 463(7281), pages 644-647, February.
    4. Gregory S. Engel & Tessa R. Calhoun & Elizabeth L. Read & Tae-Kyu Ahn & Tomáš Mančal & Yuan-Chung Cheng & Robert E. Blankenship & Graham R. Fleming, 2007. "Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems," Nature, Nature, vol. 446(7137), pages 782-786, April.
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