Nanotube-Mediated Path to Protocell Formation

Abstract

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. protocell | biomembrane | lipid nanotube | origin of life 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.

Rapid growth and fusion of protocells in surface-adhered membrane networks

“…The main driving force for the transformation of the nanotubes to protocellular compartments is the minimization of membrane curvature. The natural growth process in the previously reported system was slow (~h) 3 . The membrane replacement rate for the spontaneous inflation of a tube to a 5 μm vesicle, was estimated the to be ca.…”

“…The reservoir spontaneously spreads on the surface in form of a circular double bilayer membrane 8 . The distal of the two stacked bilayers (upper bilayer with respect to the surface), ruptures due to continuous tensile stress 8 , resulting in formation of a network of nanotubes on the proximal bilayer 3 . Fragments of the nanotubes swell over time, and form unilamellar vesicular compartments.…”

“…Fragments of the nanotubes swell over time, and form unilamellar vesicular compartments. The autonomous transformation of lipid reservoirs into networks of surface-adhered protocells interconnected by lipid nanotubes, has been described in Köksal et al 3 .…”

“…The lipid nanotube network on a solid supported bilayer was formed as described earlier 3 . Briefly, a stock suspension of multilamellar lipid reservoirs containing 50% soybean polar lipid extract, 49% E. coli polar lipid extract and 1% Rhodamine-PE or Cy5-PE were prepared by the dehydration/rehydration method 45 .…”

“…In the former study, which was conducted at constant room temperature, the protocell nucleation and growth is a slow process occurring over the course of hours to days 3 . Under natural conditions, fluctuations in temperature are expected, the impact of which on the reported system has not been considered.…”