Entropic depletion of macromolecular solutes induces symmetry-breaking surface wrinkling in myelin figures.

Abstract

Smectic liquid crystals, including multilamellar stacked lipid bilayers, strongly resist compression along the normal layer but bend readily. When mechanically stressed-such as by dehydration, osmotic stress, physical confinement, or even electric fields-they release elastic compressive energy by buckling into undulatory surface patterns reminiscent of the well-known Helfrich-Hurault instability. Although documented extensively for lamellar liquid crystals, observations of the Helfrich-Hurault instability in cylindrical smectic liquid crystals are scant. Here, we investigate the behavior of myelin figures-cylindrical smectic-A liquid crystals consisting of thousands of concentric amphiphilic bilayer lamellae separated by aqueous channels-when subjected to mechanical compression by the hyperosmotic stress from the osmolyte-laden surrounding bath. We find that the colligative ideal osmotic pressure exerted by small molecular osmolytes alone is insufficient to induce long-lived, surface instabilities. Using real-time optical and confocal fluorescence microscopy, we show that exposure to hypertonic solutions of low-molecular-weight osmolytes (<i>e.g.</i>, sucrose and glycerol) leaves myelin surfaces largely smooth, even at elevated osmotic pressures. By contrast, solutions containing macromolecular osmolytes such as polyethylene glycol and dextran trigger pronounced symmetry-breaking surface instabilities in bundles of juxtaposed myelins. These instabilities manifest as long-wavelength, quasi-sinusoidal corrugations that propagate axially and preferentially localize at inter-myelin interfaces. Quantitative analysis reveals that the wavelength and amplitude of the corrugations depend on osmolyte size, even at nominally identical osmotic pressures, further implicating excluded-volume effects. Fluorescently labeled osmolytes are excluded from corrugated interfacial regions, supporting a depletion-driven mechanism. We propose that macromolecular osmolytes generate colligatively non-ideal osmotic stresses and entropic depletion forces that stabilize interlocking surface undulations by increasing the free volume available to the depletants. These findings identify solute entropy and excluded-volume interactions as key drivers that stabilize Helfrich-Hurault-type undulatory instabilities in cylindrical smectics. They further suggest a general physical mechanism by which macromolecular crowding can induce large-scale structural remodeling in soft, multilamellar systems relevant to both synthetic materials and biological assemblies.