Molecular photoswitches mediating the strain-driven disassembly of supramolecular tubules

Abstract

Chemists have created molecular machines and switches with specific mechanical responses that were typically demonstrated in solution, where mechanically relevant motion is dissipated in the Brownian storm. The next challenge consists of designing specific mechanisms through which the action of individual molecules is transmitted to a supramolecular architecture, with a sense of directionality. Cellular microtubules are capable of meeting such a challenge. While their capacity to generate pushing forces by ratcheting growth is well known, conversely these versatile machines can also pull microscopic objects apart through a burst of their rigid tubular structure. One essential feature of this disassembling mechanism is the accumulation of strain in the tubules, which develops when tubulin dimers change shape, triggered by a hydrolysis event. We envision a strategy toward supramolecular machines generating directional pulling forces by harnessing the mechanically purposeful motion of molecular switches in supramolecular tubules. Here, we report on wholly synthetic, water-soluble, and chiral tubules that incorporate photoswitchable building blocks in their supramolecular architecture. Under illumination, these tubules display a nonlinear operation mode, by which light is transformed into units of strain by the shape changes of individual switches, until a threshold is reached and the tubules unleash the strain energy. The operation of this wholly synthetic and stripped-down system compares to the conformational wave by which cellular microtubules disassemble. Additionally, atomistic simulations provide molecular insight into how strain accumulates to induce destabilization. Our findings pave the way toward supramolecular machines that would photogenerate pulling forces, at the nanoscale and beyond.artificial molecular switches | supramolecular polymers | supramolecular machines | light

Mechanistic Insights into the Self‐Assembly of an Acid‐Sensitive Photoresponsive Supramolecular Polymer

“…The absence of any significant hypsochromic shifts demonstrates that the L 1 :TFA pairs remain stable upon UV irradiation without disassembly into the free ligand L 1 . However, the fact that marked hyperchromic UV/Vis absorption changes are observed upon UV irradiation (Figure a) are in accordance with a possible strain‐driven disassembly . Further keeping the solution at 298 K for 3 hours in the dark showed a decrease in absorbance without negligible shifts, indicating a reconstruction of the aggregates.…”

Artificial microtubules burst with energy

“…Storing energy in the form of strain build-up is difficult to achieve because in an equilibrium state, a locally high concentration of the disrupting cis form would be exchanged by trans building block from the solvent. By operating in water, a medium in which the cis building blocks are very poorly soluble, Fredy et al (2) were able to prevent such exchange, allowing the system to operate out of equilibrium. Notably, this process reflects the natural disassembly of cytoskeletal microtubules because irradiation does not immediately affect microtubule length while strain is accumulating, as was supported by simulations.…”

“…force is currently not converted into work, cytoskeletal microtubule disassembly has previously been employed to move cargo (16); a similar application for the system designed by Fredy et al (2) can easily be envisioned. Furthermore, the out-of-equilibrium state of these assemblies might be utilized in the development of synthetic systems with life-like properties.…”

“…To understand the dynamics of the living cell, as well as to create increasingly complex artificial systems, chemists strive to construct artificial molecular motors and machines. In PNAS, Fredy et al (2) present an innovative design that combines molecular motion with supramolecular chemistry to build a light-powered self-assembled machine in which energy is accumulated and released. This induces a mechanical effect that mimics the pulling force of microtubule disassembly.…”

Photoresponsive Circular Supramolecular Polymers: A Topological Trap and Photoinduced Ring‐Opening Elongation

“…v) A combination of UV light and agood (polar) solvent causes ring opening and subsequent reorganization into SP ext . utilizing the intrinsic curvature to prepare helically folded long supramolecular polymers (SP helical )b yi ntroducing an azobenzene photoresponsive chromophore [24][25][26][27][28][29] as an additional p-surface (compound 2,F igure 1a,bi). [22] We further demonstrated that the SP helical structure could be unfolded into an extended linear topology (SP ext )upon irradiation with UV light (Figure 1bii).…”