Near-Atomic Resolution Structure of J-aggregated Helical Light Harvesting Nanotubes

Abstract

Function-oriented design of supramolecular self-assemblies represents a foundational goal in chemistry. Especially, chromophore self-assemblies display extreme photophysical changes from their monomers that are sensitive to the nanoscale molecular arrangements. Slip-stacked arrangements in J-aggregates lead to red shifts (>200 nm) and enhanced quantum yields. Actively introducing specific molecular arrangements using supramolecular chemistry provides a platform to tune the excitonic couplings and avail exotic photophysical properties. However, the nanoscale molecular arrangements have not yet been directly observed in these solution-state assemblies. Here, we present a high-resolution structure of the prototypical biomimetic light harvesting nanotubes (LHNs) of an amphiphilic cyanine dye (C8S3-Cl). We achieve a 3.3 Å resolution with helical reconstruction of cryo-EM images, directly visualizing the atomic scale parameters and packing arrangements that control the excitonic properties. Our structure clearly shows a brick layer arrangement of the molecules as opposed to the previously thought herringbone arrangement. Furthermore, we identify a new non-biological supramolecular motif – interlocking sulfonates, that may be responsible for the slip-stacked packing and ultimately the J-aggregate nature of LHNs. This motif may be relevant towards other amphiphilic self-assemblies, in general and provides a new chemical handle on predictable self-assemblies.

Watching Molecular Nanotubes Self-Assemble in Real Time

“…The adsorbed molecules move around on the IW surface and rotate to form patches of recovering OW (see Figure ). Within each patch, the molecules are locally ordered into a brickwork structure, consistent with the recently resolved experimental packing motif . Depending on its size, an isolated patch can move and rotate on the surface of the IW, until it encounters other patches.…”

“…Prior to microfluidic flash-dilution, C8S3 DWNTs are characterized by two prominent narrow absorption peaks at ∼17,000 and ∼16,700 cm –1 (Figure B), which are associated with exciton transitions in the OWs and IWs, respectively, , and are polarized parallel to the long tubular axis . Meanwhile, higher-lying transitions >17,200 cm –1 have overlapping contributions from both walls and contain both parallel and perpendicularly polarized transitions. , Cryo-TEM imaging showed that the DWNTs have outer and inner diameters of 13.5 ± 0.4 and 6.9 ± 0.3 nm, respectively, and tube lengths up to several μm, which is consistent with previous results. , …”

“…This research provides a new platform that allows studying of molecular self-assembly processes of supramolecular structures in real time. A system that lends itself to this study is the C8S3-based double-walled nanotube (DWNT), the vast interest in which is driven by its close resemblance to the light-harvesting antennae in green sulfur bacteria, , with potential applications as a long-range energy transport wire in photovoltaics. , The C8S3 DWNT has an inner (outer) diameter of ∼7 nm (∼14 nm) with lengths extending several microns , and consists of hundreds of thousands of tightly packed dye molecules. − This system is uniquely suited for a controlled study of self-assembly as its outer wall can be readily removed by breaking the molecular interactions between the inner and outer walls through the addition of a water/methanol mixture (the process known as flash-dilution , ), leaving the intact inner wall as a template for subsequent reassembly of the outer wall. Furthermore, as the DWNT consists of highly absorbing/fluorescing dye molecules, the reassembly process can be conveniently tracked by optical spectroscopy, which provides access to fleeting reassembly stages.…”

Exploring the design of superradiant J-aggregates from amphiphilic monomer units

“…Prior work on molecules 1a and 1b has shown that the two primary aggregate absorption features occur from the assembly of long double-walled nanotubes (DWNT) and the subsequent bundling of those nanotubes resulting in fibers of overlapping single-walled nanotubes. 27,[35][36][37] The DWNT produces several absorption peaks, with primary features at 599 and 589 nm, corresponding to the parallel transition of the inner and outer walls of the tube respectively. 27,38 Additionally, both the inner and outer wall show auxiliary features which have been assigned to the other parallel and perpendicular excitonic transitions, which are indicative of macroscopic exciton delocalization around each tubular structure.…”

“…We refer to these as a kinetic intermediate (KI) and bundles, though the analogous behaviour of 1a suggests that the KI are transiently formed double-walled nanotubes (vide infra). 27,35 We employed non-negative matrix factorization (NNMF), an algorithm which estimates the basis spectra corresponding to each species in the binary solution, (Fig. 1d) of the concentration series data in Fig.…”