Oscillatory phase separation in giant lipid vesicles induced by transmembrane osmotic differentials

• Published in: eLife Vol. 3; p. e03695
• Main Authors: Oglęcka, Kamila, Rangamani, Padmini, Liedberg, Bo, Kraut, Rachel S, Parikh, Atul N
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 15.10.2014; eLife Sciences Publications, Ltd
• Subjects: Animals; BASIC BIOLOGICAL SCIENCES; Biophysics and Structural Biology; Cell Biology; Chickens; compartmentalization; giant phospholipid vesicle; Hypertonic Solutions - pharmacology; Hypotonic Solutions - pharmacology; Life Sciences & Biomedicine - Other Topics; Lipid Bilayers - chemistry; lipid raft; Lipids; Materials science; Microscopy; Oscillations; Osmosis; Osmosis - drug effects; Osmotic pressure; Permeability - drug effects; phase separation; Phase Transition - drug effects; Phase transitions; Porosity; primitive osmoregulation; Shells; Solutes; Sucrose; Temperature; Unilamellar Liposomes - chemistry; Vesicles; United States > US; California; lipid rafts; phase separation; cell biology; giant phospholipid vesicles; compartmentalization; structural biology; primitive osmoregulation; biophysics
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.03695

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. All living cells are surrounded by a membrane that water can pass through. However, water often contains other molecules called solutes, and many of these cannot pass through the cell membrane. If the concentration of solutes outside the cell is, say, suddenly decreased, then water molecules will tend to move into the cell to lower the solute concentration there. This process, which is called osmosis, strives to equalize the solute concentrations inside and outside the cell. Osmosis can have dramatic consequences for cells. Animal cells need to be bathed in water to survive, but if the solute concentration outside a cell is higher than inside, the cell can lose a lot of water and die. And if the solute concentration outside is lower, then water enters the cell and it can burst. Single celled microbes use a variety of strategies to counter the movement of water by osmosis: strong cell walls prevent the cell from swelling too much, and channel proteins in the membrane can be opened to allow solutes to pass through. But it is not known how more primitive cells—cells that lived billions of years ago—might have responded to fluctuations in their environment. Oglęcka et al. have now used artificial membranes to make closed compartments called giant vesicles that mimic certain properties of cells. When giant vesicles are filled with a sugar solution and placed in water with a lower concentration of sugar, a series of events takes place that can lead to the sugar concentration inside and outside the vesicle becoming more equal. At first the vesicle expands as water enters. However, as the membrane stretches, a temporary hole opens up, which allows some of the excess solute molecules and water to escape, shrinking the vesicle. This sets up cycles of vesicle expansion and contraction that gradually lead to the solute concentrations on both sides of the membrane becoming more equal. This cyclical expansion and contraction of the vesicle also changes the membrane, decorating it with “domains” of specialized molecules, when expanded and uniform, when shrunk. It is possible that this process may have helped the first primitive cells to survive and, maybe, even benefit from changes in solute concentration in their environment.