Transient pearling and vesiculation of membrane tubes under osmotic gradients

Abstract

We report the experimental observation of osmotically induced transient pearling instabilities in vesicular membranes. Giant phospholipid vesicles subjected to negative osmotic gradient, which drives the influx of water in to the vesicular interior, produces transient cylindrical protrusions. These protrusions exhibit a remarkable pearling intermediate, which facilitates their subsequent retraction. The pearling front propagates from the distal free end of the protrusion toward the vesicular source and accompanies gradual shortening of the protrusion via pearl-pearl coalescence. Real-time introduction of a positive osmotic gradient, on the other hand, drives vigorous shape fluctuations, which in turn produce cylindrical, prolate- and pear-shaped intermediates presumably due to an increased vesicular area relative to the encapsulated volume. These intermediates transiently produce a pearled state prior to their fission. In both cases, the transient pearling state gives rise to an array of stable spherical daughter vesicles, which may be connected to one another by fine tethers not resolved in our experiments. These results may have implications for self-reproduction in primitive, protein-free, cells.

Chemotactic Amoeboid-Like Shape Change of a Vesicle under a pH Gradient

“…In this study, the direction of the extrusion was controlled by the pH gradient. This is quite different from the monotonic extrusion in POPC (1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine) vesicles, 18 in which the extrusion direction appeared to be random. Vesicles that exhibit the oscillatory generation of a pseudopod-like structure owing to the surrounding pH may lead to the design of molecular assemblies that mimic amoeboid motion.…”

“…However, pseudopod contraction was not observed after the extrusion (see SI Figure S4-3). Almost all vesicles under 1 M NaOH diffusion exhibited pearling 18 instability after extrusion. Figure 2b shows vesicle transformation under diffusion of 1 M NaCl.…”

“…Sanborn et al reported that under sucrose diffusion, vesicles composed of 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine (POPC), sphingomyelin, and cholesterol formed irreversible extrusions that exhibited pearling instability. 18 This transformation was explained by the osmotic pressure difference across the vesicle membrane caused by the addition of sucrose outside the vesicle. 18 To adjust for the osmotic pressure difference, the water inside the vesicle was extracted to the outside, increasing the specific surface area of the vesicle and resulting in the vesicle transformation.…”

“…18 This transformation was explained by the osmotic pressure difference across the vesicle membrane caused by the addition of sucrose outside the vesicle. 18 To adjust for the osmotic pressure difference, the water inside the vesicle was extracted to the outside, increasing the specific surface area of the vesicle and resulting in the vesicle transformation. In the present study, the extrusion of vesicles under the diffusion of 1 M NaCl and NaOH was attributed to the same mechanism as the one proposed for the POPC vesicle.…”

“…This extrusion and contraction cycle was repeated many times, and the elongated parts occasionally exhibited pearling instability. The extrusion of the cylindrical structure and pearling instability were discussed based on an osmotic pressure difference across the membrane; this type of shape change attracts special interest, 18 and the dynamics are essentially a monotonic relaxation towards the local equilibrium. 18,19 However, to the best of the authors' knowledge, oscillatory shape changes comprised of extrusion and contraction have not been reported to date.…”