Kalra Aarat P, Benny Alfy, Travis Sophie M, Zizzi Eric A, Morales-Sanchez Austin, Oblinsky Daniel G, Craddock Travis J A, Hameroff Stuart R, MacIver M Bruce, Tuszyński Jack A, Petry Sabine, Penrose Roger, Scholes Gregory D
Department of Chemistry, New Frick Chemistry Building, Princeton University, Princeton, New Jersey08544, United States.
Department of Molecular Biology, Schultz Laboratory, Princeton University, Princeton, New Jersey08544, United States.
ACS Cent Sci. 2023 Jan 12;9(3):352-361. doi: 10.1021/acscentsci.2c01114. eCollection 2023 Mar 22.
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.
微管蛋白二聚体的重复排列赋予微管极大的机械强度，微管在细胞内用作大分子运输的支架，并在生物混合装置中得到应用。微管中的晶体结构，其晶格常数短到足以使氨基酸发色团之间发生能量转移，这与为光捕获设计的合成结构相似。光激发后，这些氨基酸发色团能否像天然或人工光捕获系统一样沿着微管转移激发能呢？在这里，我们使用色氨酸自身荧光寿命来探测微管蛋白和微管中芳香族残基之间的能量跳跃。通过研究猝灭剂浓度如何改变色氨酸自身荧光寿命，我们证明电子能量可以在微管中扩散6.6纳米。我们发现，虽然扩散长度受微管蛋白聚合状态（游离微管蛋白与微管晶格中的微管蛋白）影响，但它们不会因原纤维的平均数量（13与14）而发生显著改变。我们还证明，麻醉剂依托咪酯和异氟烷的存在会减少激子扩散。传统弗斯特理论（考虑色氨酸和酪氨酸残基之间的相互作用）所解释的能量传输并不能充分解释我们的观察结果。我们的研究表明，出乎意料的是，微管是有效的光捕获器。
