Abstract
Giant lipid vesicles are closed compartments consisting of semi-permeable shells, which isolate femto- to pico-liter quantities of aqueous core from the bulk. Although water permeates readily across vesicular walls, passive permeation of solutes is hindered. In this study, we show that, when subject to a hypotonic bath, giant vesicles consisting of phase separating lipid mixtures undergo osmotic relaxation exhibiting damped oscillations in phase behavior, which is synchronized with swell-burst lytic cycles: in the swelled state, osmotic pressure and elevated membrane tension due to the influx of water promote domain formation. During bursting, solute leakage through transient pores relaxes the pressure and tension, replacing the domain texture by a uniform one. This isothermal phase transition--resulting from a well-coordinated sequence of mechanochemical events--suggests a complex emergent behavior allowing synthetic vesicles produced from simple components, namely, water, osmolytes, and lipids to sense and regulate their micro-environment.
Highlights
Giant unilamellar vesicles (GUVs) are the simplest cell-like closed compartments consisting of semipermeable flexible shells (4–6 nm thick, 5–50 μm diameter), isolating femto- to pico-liter quantities of aqueous core from the surrounding bulk (Walde et al, 2010)
In the work reported here, we show that the swell–burst cycles in hypertonic vesicles consisting of domain-forming lipid mixtures (Baumgart et al, 2003; Veatch and Keller, 2005) become coupled with the membrane's compositional degrees of freedom, producing a long-lived transient response characterized by damped oscillations in phase behavior at the membrane surface, cycling between the state characterized by large microscopic domains at the membrane surface and an optically uniform one. This oscillatory phase separation occurs isothermally, and it is driven by a sequence of elementary biophysical processes involving cyclical changes in osmotic pressure, membrane tension, and poration, which attend swell–burst cycles (Koslov and Markin, 1984; Mui et al, 1993; Popescu and Popescu, 2008): in the swelled state, osmotic pressure and elevated membrane tension due to the influx of water promote the appearance of microscopic domains (Akimov et al, 2007; Ayuyan and Cohen, 2008; Hamada et al, 2011)
The GUVs (Morales-Penningston et al, 2010) we investigated consist of ternary lipid mixtures composed of cholesterol (Ch), sphingomyelin (SM), and the unsaturated phospholipid, POPC (1-palmitoyl2-oleoyl-sn-1-glycero-3-phosphocholine) at room temperature (25°C) (‘Materials and methods’)
Summary
Giant unilamellar vesicles (GUVs) are the simplest cell-like closed compartments consisting of semipermeable flexible shells (4–6 nm thick, 5–50 μm diameter), isolating femto- to pico-liter quantities of aqueous core from the surrounding bulk (Walde et al, 2010). A consequence of the osmotic influx of water in vesicles embedded in hypotonic media is the buildup of lateral membrane tension due to changes in the balance of forces within the bilayer producing high energy states (compared to isotonic relaxed vesicles) (Needham and Nunn, 1990).
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