Electronic Energy Migration in Microtubules

TL;DR

This study reveals that microtubules can transfer excitation energy over nanometer scales, acting as natural light-harvesting structures, with energy diffusion affected by polymerization state and anesthetic presence.

Contribution

It demonstrates that microtubules facilitate electronic energy transfer through tryptophan chromophores, challenging conventional F"orster theory explanations and highlighting their potential as biohybrid light-harvesting systems.

Findings

Energy diffuses over 6.6 nm in microtubules.

Diffusion length varies with tubulin polymerization state.

Anesthetics like etomidate and isoflurane reduce exciton diffusion.

Abstract

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 inter-tryptophan energy hopping in tubulin and microtubules. By studying how 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 F\"orster 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.