A nanotube-mediated path to protocell formation

Cellular compartments are membrane-enclosed, spatially distinct microenvironments which confine and protect biochemical reactions in the biological cell. On the early Earth, the autonomous formation of compartments is thought to have led to the encapsulation of nucleotides, thereby satisfying a starting condition for the emergence of life. Recently, surfaces have come into focus as potential platforms for the self-assembly of prebiotic compartments, as significantly enhanced vesicle formation was reported in the presence of solid interfaces. The detailed mechanism of such formation at the mesoscale is still under discussion. We report here on the spontaneous transformation of solid surface-adhered lipid deposits to unilamellar membrane compartments through a straightforward sequence of topological changes, proceeding via a network of interconnected lipid nanotubes. We show that this transformation is entirely driven by surface-free energy minimization and does not require hydrolysis of organic molecules, or external stimuli such as electrical currents or mechanical agitation. The vesicular structures take up and encapsulate their external environment during formation, and can subsequently separate and migrate upon exposure to hydrodynamic flow. This may link, for the first time, the self-directed transition from weakly organized bioamphiphile assemblies on solid surfaces to protocells with secluded internal contents.SignificanceThe nature of the physical and chemical mechanisms behind the formation, growth and division of the earliest protocells is among the key questions concerning the origin of life. Establishing a simple pathway for the assembly of protocell structures from the primordial soup is a particular challenge. Emerging evidence supporting the assumption that solid surfaces have a governing role in protocell formation has recently expanded the scope, and created new inspiration for investigation. By presenting a physical path from self-assembled amphiphile-based membranes on solid surfaces to spherical single-membrane compartments via a consistent sequence of transformations, solely driven by the materials properties of the interfaces, a direct link between the presence of functional biomolecules and the development of protocells can be established.