Simple sugars shape giant vesicles into multispheres with many membrane necks

Abstract

Simple sugars such as glucose and sucrose are ubiquitous in all organisms. One remarkable property of these small solutes is their ability to protect biomembranes against dehydration damage. This property, which reflects the underlying sugar–lipid interactions, has been intensely studied for lipid bilayers interacting with a single sugar at low hydration. Here, we use giant vesicles to investigate fully hydrated lipid membranes in contact with two sugars, glucose and sucrose. The vesicles were osmotically balanced, with the same total sugar concentration in the interior and exterior aqueous solutions. However, the two solutions differed in their composition: the interior solution contained only sucrose whereas the exterior one contained primarily glucose. This sugar asymmetry generated a striking variety of multispherical or “multi-balloon” vesicle shapes. Each multisphere involved only a single membrane that formed several spherical segments, which were connected by narrow, hourglass-shaped membrane necks. These morphologies revealed that the sugar–lipid interactions generated a significant spontaneous curvature with a magnitude of about 1 μm⁻¹. Such a spontaneous curvature can be generated both by depletion and by adsorption layers of the sugar molecules arising from effectively repulsive and attractive sugar–lipid interactions. All multispherical shapes are stable over a wide range of parameters, with a substantial overlap between the different stability regimes, reflecting the rugged free energy landscape in shape space. One challenge for future studies is to identify pathways within this landscape that allow us to open and close the membrane necks of these shapes in a controlled and reliable manner. We will then be able to apply these multispheres as metamorphic chambers for chemical reactions and nanoparticle growth.