Colony-like Protocell Superstructures

Abstract

We report the formation, growth, and dynamics of model protocell superstructures on solid surfaces, resembling single cell colonies. These structures, consisting of several layers of lipidic compartments enveloped in a dome-shaped outer lipid bilayer, emerged as a result of spontaneous shape transformation of lipid agglomerates deposited on thin film aluminum surfaces. Collective protocell structures were observed to be mechanically more stable compared to isolated spherical compartments. We show that the model colonies encapsulate DNA and accommodate nonenzymatic, strand displacement DNA reactions. The membrane envelope is able to disassemble and expose individual daughter protocells, which can migrate and attach via nanotethers to distant surface locations, while maintaining their encapsulated contents. Some colonies feature "exocompartments", which spontaneously extend out of the enveloping bilayer, internalize DNA, and merge again with the superstructure. A continuum elastohydrodynamic theory that we developed suggests that a plausible driving force behind subcompartment formation is attractive van der Waals (vdW) interactions between the membrane and surface. The balance between membrane bending and vdW interactions yields a critical length scale of 236 nm, above which the membrane invaginations can form subcompartments. The findings support our hypotheses that in extension of the "lipid world hypothesis", protocells may have existed in the form of colonies, potentially benefiting from the increased mechanical stability provided by a superstructure.