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.
Highlights
Since the discovery of coherent wave behavior stimulating excitonic transport in natural photosynthetic systems under ambient conditions [1, 2], ample motivation has arisen to investigate the relevance of quantum mechanical behavior in diverse biological networks of photoactive molecules
The positions and orientations of the dipoles of the tryptophan molecules have been obtained in previous works by molecular dynamics simulations and quantum chemistry calculations and have closely reproduced experimental spectra for the tubulin heterodimeric protein [26]
Analyzing the properties of a microtubule of length L ∼ 800 nm, which is larger than the wavelength of the excitation transition (L > λ = 280 nm), requires an approach that goes beyond the transition dipole-dipole couplings alone
Summary
Since the discovery of coherent wave behavior stimulating excitonic transport in natural photosynthetic systems under ambient conditions [1, 2], ample motivation has arisen to investigate the relevance of quantum mechanical behavior in diverse biological networks of photoactive molecules. The main question we address in this paper is whether the arrangement of photoactive molecules in the microtubule structure can support extended excitonic states with a giant dipole strength, at least in the absence of environmental disorder Such extended states, if robust to noise, can support efficient transport of photoexcitations, which could have a biological role in microtubule signaling between cells and across the brain [26]. The advantage of this formalism, with respect to the simple dipole-dipole interaction commonly used in the literature, is that it allows us to consider system sizes that are even larger than the wavelength of the absorbed light This property becomes important for large biopolymeric structures like microtubules whose length is generally several orders of magnitude larger than the wavelength associated with the molecular transitions (λ = 280 nm).
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