Near-atomic-resolution structure of J-aggregated helical light-harvesting nanotubes

• Published in: Nature chemistry 2024-05, Vol.16 (5), p.800-808
• Main Authors: Deshmukh, Arundhati P., Zheng, Weili, Chuang, Chern, Bailey, Austin D., Williams, Jillian A., Sletten, Ellen M., Egelman, Edward H., Caram, Justin R.
• Format: Article
• Language: English
• Subjects: 639/638/440/527; 639/638/541/966; 639/638/563; Aggregates; Analytical Chemistry; Assemblies; Atomic structure; Biochemistry; Biomimetics; Bricks; Chemistry; Chemistry and Materials Science; Chemistry/Food Science; Chromophores; Couplings; Cyanine dyes; Electron microscopy; Energy; High resolution; Inorganic Chemistry; Light; Locking; Microscopy; Nanotechnology; Nanotubes; NMR; Nuclear magnetic resonance; Organic Chemistry; Physical Chemistry; Structure-function relationships; Sulfonates
• ISSN: 1755-4330; 1755-4349
• DOI: 10.1038/s41557-023-01432-6

Cryo-electron microscopy has delivered a resolution revolution for biological self-assemblies, yet only a handful of structures have been solved for synthetic supramolecular materials. Particularly for chromophore supramolecular aggregates, high-resolution structures are necessary for understanding and modulating the long-range excitonic coupling. Here, we present a 3.3 Å structure of prototypical biomimetic light-harvesting nanotubes derived from an amphiphilic cyanine dye (C8S3-Cl). Helical 3D reconstruction directly visualizes the chromophore packing that controls the excitonic properties. Our structure clearly shows a brick layer arrangement, revising the previously hypothesized herringbone arrangement. Furthermore, we identify a new non-biological supramolecular motif—interlocking sulfonates—that may be responsible for the slip-stacked packing and J-aggregate nature of the light-harvesting nanotubes. This work shows how independently obtained native-state structures complement photophysical measurements and will enable accurate understanding of (excitonic) structure–function properties, informing materials design for light-harvesting chromophore aggregates. Chromophore supramolecular assemblies have long been studied for their exotic photophysical properties arising from their local geometry and long-range sensitive excitonic couplings. Now a high-resolution structure of a model nanotubular system has revealed a uniform brick-layer molecular arrangement and a non-biological supramolecular motif—interlocking sulfonates—enabling clear understanding of supramolecular structure–excitonic property relationships.