Electronic Energy Migration in Microtubules

Author: Aarat P Kalra1, Alfy Benny1, Sophie M Travis2, Eric A Zizzi3, Austin Morales-Sanchez1, Daniel G Oblinsky1, Travis J A Craddock4, Stuart R Hameroff5, M Bruce MacIver6, Jack A Tuszyński3,7,8, Sabine Petry2, Roger Penrose9, Gregory D Scholes1
1 Department of Chemistry, New Frick Chemistry Building, Princeton University, Princeton, New Jersey08544, United States.
2 Department of Molecular Biology, Schultz Laboratory, Princeton University, Princeton, New Jersey08544, United States.
3 Department of Mechanical and Aerospace Engineering (DIMEAS), Politecnico di Torino, Torino10129, Italy.
4 Departments of Psychology & Neuroscience, Computer Science, and Clinical Immunology, Nova Southeastern University, Ft. Lauderdale, Florida33314, United States.
5 Department of Anesthesiology, Center for Consciousness Studies, University of Arizona, Tucson, Arizona85721, United States.
6 Department of Anesthesiology, Stanford University School of Medicine, Stanford, California94305, United States.
7 Department of Physics, University of Alberta, Edmonton, AlbertaT6G 2E1, Canada.
8 Department of Oncology, University of Alberta, Edmonton, AlbertaT6G 1Z2, Canada.
9 Mathematical Institute, Andrew Wiles Building, University of Oxford, Radcliffe Observatory Quarter, Woodstock Road, Oxford, OX2 6GG, United Kingdom.
Conference/Journal: ACS Cent Sci
Date published: 2023 Jan 12
Other: Volume ID: 9 , Issue ID: 3 , Pages: 352-361 , Special Notes: doi: 10.1021/acscentsci.2c01114. , Word Count: 200

The repeating arrangement of tubulin dimers confers great mechanical strength to microtubules, which are used as scaffolds for intracellular macromolecular transport in cells and exploited in biohybrid devices. The crystalline order in a microtubule, with lattice constants short enough to allow energy transfer between amino acid chromophores, is similar to synthetic structures designed for light harvesting. After photoexcitation, can these amino acid chromophores transfer excitation energy along the microtubule like a natural or artificial light-harvesting system? Here, we use tryptophan autofluorescence lifetimes to probe energy hopping between aromatic residues in tubulin and microtubules. By studying how the quencher concentration alters tryptophan autofluorescence lifetimes, we demonstrate that electronic energy can diffuse over 6.6 nm in microtubules. We discover that while diffusion lengths are influenced by tubulin polymerization state (free tubulin versus tubulin in the microtubule lattice), they are not significantly altered by the average number of protofilaments (13 versus 14). We also demonstrate that the presence of the anesthetics etomidate and isoflurane reduce exciton diffusion. Energy transport as explained by conventional Förster theory (accommodating for interactions between tryptophan and tyrosine residues) does not sufficiently explain our observations. Our studies indicate that microtubules are, unexpectedly, effective light harvesters.

PMID: 36968538 PMCID: PMC10037452 DOI: 10.1021/acscentsci.2c01114