Cited by 56Spectroscopy and Quantum Chemical StudiesStrong Light-Matter InteractionsPhotochemistry and Electron Transfer Studies

On the existence of superradiant excitonic states in microtubules

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Celardo, G L, Angeli, M, Craddock, T J A, Kurian, P·2019·New Journal of Physics

Abstract

Microtubules are biological protein polymers with critical and diverse functions. Their structures share some similarities with photosynthetic antenna complexes, particularly in the ordered arrangement of photoactive molecules with large transition dipole moments. As the role of photoexcitations in microtubules remains an open question, here we analyze tryptophan molecules, the amino acid building block of microtubules with the largest transition dipole strength. By taking their positions and dipole orientations from realistic models capable of reproducing tubulin experimental spectra, and using a Hamiltonian widely employed in quantum optics to describe light–matter interactions, we show that such molecules arranged in their native microtubule configuration exhibit a superradiant lowest exciton state, which represents an excitation fully extended on the chromophore lattice. We also show that such a superradiant state emerges due to supertransfer coupling between the lowest exciton states of smaller blocks of the microtubule. In the dynamics we find that the spreading of excitation is ballistic in the absence of external sources of disorder and strongly dependent on initial conditions. The velocity of photoexcitation spreading is shown to be enhanced by the supertransfer effect with respect to the velocity one would expect from the strength of the nearest-neighbor coupling between tryptophan molecules in the microtubule. Finally, such structures are shown to have an enhanced robustness to static disorder when compared to geometries that include only short-range interactions. These cooperative effects (superradiance and supertransfer) may induce ultra-efficient photoexcitation absorption and could enhance excitonic energy transfer in microtubules over long distances under physiological conditions.

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  • The non-Hermitian Hamiltonian approach has been used to develop a theoretical model for exciton transport within microtubules.

    “The non-Hermitian Hamiltonian approach outlined above has been recently utilized in Ref. [61] to develop a theoretical model for exciton transport within microtubules.”
  • Superradiance in microtubules demonstrates robustness to disorder, even with uniformly distributed excitation energy across Trp dipole sites.

    “the superradiance demonstrated robustness to disorder, even with uniformly distributed excitation energy across Trp dipole sites.”
  • The ground state of a whole microtubule segment acts as a coherent superposition of the ground states of its smaller components.

    “The same probability-based analysis using smaller microtubule segments (specific groups of 13 coupled spirals, the minimum number ensuring the superradiant state as the lowest excitonic state) showed that the ground state of the whole segment acts as a coherent superposition of the ground states of its smaller components.”
  • Photoexcitation spreads ballistically along the longitudinal axis of microtubule segments.

    “Furthermore, photoexcitation was found to spread ballistically along the longitudinal axis”
  • In the model of Ref. [61], aromatic tryptophan amino acids have the largest transition dipole moment in the structure of microtubules.

    “In this model, aromatic tryptophan amino acids (Trp)—that have the largest transition dipole moment in the structure of microtubules—were treated as the photoactive molecular sites through which a single exciton delocalizes.”

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References 71 · Cited by 56

Research works printed but not linked: 4

  1. Eisenberg I et al 2014 Phys. Chem. Chem. Phys. 16 11196 · DOI
  2. Yuen-Zhou J et al 2014 ACS Nano 8 5527 · DOI
  3. Hu X, Damjanovic A, Ritz T and Schulten K 1998 Proc. Natl Acad. Sci. USA 95 5935 · DOI
  4. Tobias Z et al 2014 New J. Phys. 16 055002 · DOI

Authors
Celardo, G. L., Angeli, M., Craddock, T. J. A., & Kurian, P.
Affiliations
  • Benemérita Universidad Autónoma de Puebla (MX)
  • Università Cattolica del Sacro Cuore (IT)
  • Nova Southeastern University (US)
  • University of Iowa (US)
Venue
New Journal of Physics
Published
2019-02-05
Volume
21
Issue
2
Pages
023005
ISSN
1367-2630 (ISSN-L)
OpenAlex
W2891802132
Cited by
56
References
71
Citations by year
2026: 14 · 2025: 10 · 2024: 10 · 2023: 4 · 2022: 11 · 2021: 2 · 2020: 4 · 2019: 1
FWCI
0.81
Type
journal article
Language
en
Open access
Locations
  • New Journal of Physics (publishedVersion, cc-by)
  • arXiv (Cornell University) (submittedVersion)
  • Florence Research (University of Florence) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • NSUWorks (Nova Southeastern University) (submittedVersion)
  • arXiv (Cornell University)
Funders
  • National Institute on Minority Health and Health Disparities (G12MD007597)
  • Nova Southeastern University President’s Faculty Research and Development Grant (PFRDG 335426)
  • US-Italy Fulbright Commission
  • PRODEP (511-6/17-8017)
  • Whole Genome Science Foundation
Topics
  • Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Spectroscopy and Quantum Chemical Studies
  • Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Strong Light-Matter Interactions
  • Physical Sciences › Chemistry › Physical and Theoretical Chemistry › Photochemistry and Electron Transfer Studies
Keywords
microtubules, superradiance, excitonic states, tryptophan, exciton transfer, photoexcitation dynamics, light-matter interaction, tubulin, transition dipole moment

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