Ions Modulate Stress-Induced Nanotexture in Supported Fluid Lipid Bilayers

Abstract

Most plasma membranes comprise a large number of different molecules including lipids and proteins. In the standard fluid mosaic model, the membrane function is effected by proteins whereas lipids are largely passive and serve solely in the membrane cohesion. Here we show, using supported 1,2-dioleoyl-sn-glycero-3-phosphocholine lipid bilayers in different saline solutions, that ions can locally induce ordering of the lipid molecules within the otherwise fluid bilayer when the latter is supported. This nanoordering exhibits a characteristic length scale of ∼20 nm, and manifests itself clearly when mechanical stress is applied to the membrane. Atomic force microscopy (AFM) measurements in aqueous solutions containing NaCl, KCl, CaCl2, and Tris buffer show that the magnitude of the effect is strongly ion-specific, with Ca2+ and Tris, respectively, promoting and reducing stress-induced nanotexturing of the membrane. The AFM results are complemented by fluorescence recovery after photobleaching experiments, which reveal an inverse correlation between the tendency for molecular nanoordering and the diffusion coefficient within the bilayer. Control AFM experiments on other lipids and at different temperatures support the hypothesis that the nanotexturing is induced by reversible, localized gel-like solidification of the membrane. These results suggest that supported fluid phospholipid bilayers are not homogenous at the nanoscale, but specific ions are able to locally alter molecular organization and mobility, and spatially modulate the membrane’s properties on a length scale of ∼20 nm. To illustrate this point, AFM was used to follow the adsorption of the membrane-penetrating antimicrobial peptide Temporin L in different solutions. The results confirm that the peptides do not absorb randomly, but follow the ion-induced spatial modulation of the membrane. Our results suggest that ionic effects have a significant impact for passively modulating the local properties of biological membranes, when in contact with a support such as the cytoskeleton.

Long-lived ionic nano-domains can modulate the stiffness of soft interfaces

“…3) imply that lipid mobility would not dramatically alter such phenomena. Indeed, similar iondependent effects have been observed on fluid bilayers 5 and in principle, these effects could occur at any soft interface, as they rely only on water molecules mediating these common ions' interaction with themselves and the lipids. At biological interfaces, we expect this mechanism to modulate the local viscoelastic properties on a timescale relevant for influencing processes such as molecular adsorption or the gating of mechanosensitive protein channels.…”

Lubricating properties of single metal ions at interfaces

“…No buffering agent was used to avoid interfering with the measurements. 56,57 Testing of the pH was also conducted immediately after conducting experiments to ensure stability.…”

Arginine‐enveloped virus inactivation and potential mechanisms

“…The positive charge and primary aliphatic amine group of Tris, as shown in Table , are thought to be the root cause of multiple interactions . Charges on molecules interact with proteins and lipids, while primary aliphatic amines interact with several compounds including DNA . Through lipid bilayer, protein, or DNA interactions, Tris is thought to synergize with arginine to inactivate enveloped viruses.…”

“…116 On the contrary to the above studies, in supported lipid bilayers, atomic force microscopy measurements demonstrated that Tris buffer reduced membrane stress, while other ions, such as Ca 2+ , increased membrane stress. 117 Though there are mixed results on the effects to lipid bilayers, Tris buffer does interact with membranes.…”

“…120 The positive charge and primary aliphatic amine group of Tris, as shown in Table 2, are thought to be the root cause of multiple interactions. 106,118,120,121 Charges on molecules interact with proteins and lipids, 117,[122][123][124][125][126] while primary aliphatic amines interact with several compounds including DNA. 106,118,120,121 3 describes pore formation by arginine, followed by further viral damage from the synergistic factor.…”