On the existence of superradiant excitonic states in microtubules

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...

Full description

Bibliographic Details
Main Authors: G L Celardo, M Angeli, T J A Craddock, P Kurian
Format: Article
Language:English
Published: IOP Publishing 2019-01-01
Series:New Journal of Physics
Subjects:
Online Access:https://doi.org/10.1088/1367-2630/aaf839
_version_ 1797750271520014336
author G L Celardo
M Angeli
T J A Craddock
P Kurian
author_facet G L Celardo
M Angeli
T J A Craddock
P Kurian
author_sort G L Celardo
collection DOAJ
description 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.
first_indexed 2024-03-12T16:30:17Z
format Article
id doaj.art-2e2203b11c634bdfbec44470d82891cb
institution Directory Open Access Journal
issn 1367-2630
language English
last_indexed 2024-03-12T16:30:17Z
publishDate 2019-01-01
publisher IOP Publishing
record_format Article
series New Journal of Physics
spelling doaj.art-2e2203b11c634bdfbec44470d82891cb2023-08-08T15:31:11ZengIOP PublishingNew Journal of Physics1367-26302019-01-0121202300510.1088/1367-2630/aaf839On the existence of superradiant excitonic states in microtubulesG L Celardo0M Angeli1T J A Craddock2P Kurian3https://orcid.org/0000-0002-4160-6434Benemérita Universidad Autónoma de Puebla , Apartado Postal J-48, Instituto de Física, 72570, MexicoInternational School for Advanced Studies (SISSA) , Via Bonomea 265, I-34136 Trieste, Italy; Dipartimento di Matematica e Fisica and Interdisciplinary Laboratories for Advanced Materials Physics, Università Cattolica del Sacro Cuore , via Musei 41, I-25121 Brescia, ItalyDepartments of Psychology and Neuroscience, Computer Science, and Clinical Immunology, Nova Southeastern University, Fort Lauderdale FL 33314, United States of America; Clinical Systems Biology Group, Institute for Neuro-Immune Medicine, Fort Lauderdale FL 33314, United States of AmericaQuantum Biology Laboratory, Howard University, Washington DC 20059, United States of America; Center for Computational Biology and Bioinformatics, Howard University College of Medicine, Washington DC 20059, United States of America; Department of Physics and Astronomy, University of Iowa, Iowa City IA 52242, United States of AmericaMicrotubules 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.https://doi.org/10.1088/1367-2630/aaf839quantum biologyquantum transport in disordered systemsopen quantum systemsenergy transfer
spellingShingle G L Celardo
M Angeli
T J A Craddock
P Kurian
On the existence of superradiant excitonic states in microtubules
New Journal of Physics
quantum biology
quantum transport in disordered systems
open quantum systems
energy transfer
title On the existence of superradiant excitonic states in microtubules
title_full On the existence of superradiant excitonic states in microtubules
title_fullStr On the existence of superradiant excitonic states in microtubules
title_full_unstemmed On the existence of superradiant excitonic states in microtubules
title_short On the existence of superradiant excitonic states in microtubules
title_sort on the existence of superradiant excitonic states in microtubules
topic quantum biology
quantum transport in disordered systems
open quantum systems
energy transfer
url https://doi.org/10.1088/1367-2630/aaf839
work_keys_str_mv AT glcelardo ontheexistenceofsuperradiantexcitonicstatesinmicrotubules
AT mangeli ontheexistenceofsuperradiantexcitonicstatesinmicrotubules
AT tjacraddock ontheexistenceofsuperradiantexcitonicstatesinmicrotubules
AT pkurian ontheexistenceofsuperradiantexcitonicstatesinmicrotubules