Permeability and line tension dependent response of polyunsaturated membranes to osmotic stresses


Shiva Emami*, Wan-Chih Su*, Sowmya Purushothaman, Viviane N. Ngassam, and Atul N. Parikh, Biophysical Journal 115, 1942-1955, 2018

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The lipidome of plant plasma membranes – enriched in cellular phospholipids containing at least one polyunsaturated fatty acid tails and a variety of phytosterols and phytosphingolipids – is adapted to significant abiotic stresses. But how mesoscale membrane properties of these membranes, such as permeability and deformability, which arise from their unique molecular compositions and corresponding lateral organization, facilitate response to global mechanical stresses is largely unknown. Here, using giant vesicles reconstituting mixtures of polyunsaturated lipids (Soy-PC), glucosylceramide (GlcCer), and sitosterol common to plant membranes, we find that the membranes adopt “janus-like” domain morphologies and display anomalous solute permeabilities. The former textures the membrane with a single sterol-GlcCer enriched, liquid-ordered (Lo-like) domain separated from a liquid-disordered (Ld-like) phase consisting primarily of Soy-PC. When subject to osmotic downshifts, the GUVs respond by transiently producing well-known swell-burst cycles. In each cycle, the influx of water swells the GUV rendering the membrane tense. Subsequent rupture of the membrane through transient poration, which localizes in the Ld-like phase or at the domain boundaries, reduces the osmotic stress by expelling some of the excess osmolytes (and solvent) before sealing. When subject to abrupt hypertonic stress, they deform by nucleating buds at the domain phase boundaries. Remarkably, this incipient vesiculation is reversed in a statistically significant fraction of GUVs because of the interplay with solute permeation time scales, which render osmotic stresses short-lived. This then suggests a novel control mechanism in which an interplay of permeability and deformability regulates osmotically induced membrane deformation and limits vesiculation-induced loss of membrane material. Interestingly, recapitulation of such dynamic morphological reconfigurability – switching between budded and non-budded morphologies – due to the interplay of membrane permeability, which temporally reverses the osmotic gradient, and domain boundaries, which selects modes of deformations, might prove valuable in enowing synthetic cells with novel morphological responsiveness.

DOI: 10.1016/j.bpj.2018.09.031