Reduction in Tension and Stiffening of Lipid Membranes in an Electric Field Revealed by X-Ray Scattering

Abstract

The effect of AC electric fields on the elasticity of supported lipid bilayers has been investigated at the microscopic level using grazing incidence synchrotron x-ray scattering. A strong decrease in the membrane tension up to 1mN/m and a dramatic increase of its effective rigidity up to 300k B T are observed for local electric potentials seen by the membrane 1V. The experimental results were analyzed using detailed electrokinetic modeling and non-linear Poisson-Boltzmann theory. Based on a modeling of the electromagnetic stress which provides an accurate description of bilayer separation vs pressure curves, we show that the decrease in tension results from the amplification of charge fluctuations on the membrane surface whereas the increase in bending rigidity results from direct interaction between charges in the electric double layer. These effects eventually lead to a destabilization of the bilayer and vesicle formation. Similar effects are expected at the tens of nanometer lengthscale in cell membranes with lower tension, and could explain a number of electrically driven processes.Electric fields can be used to destabilize lipid bilayers as in the electroformation process, the most popular method to form large unilamellar vesicles [1], or to manipulate the shape of vesicles [2][3][4]. Beyond biosensor applications and the investigation of fundamental mechanical, dynamical and binding properties of membranes using impedance spectroscopy or dielectric relaxation [5], the strong influence of electric fields on lipid membrane behavior is also used in numerous applications in cell biology, biotechnology and pharmacology [6, 7] such as cell hybridization [8], electroporation [9], electrofusion [10] and electropermeabilization [11]. All these effects imply a strong deformation of the membranes in the field, the understanding of which in terms of elastic properties is therefore of prime importance [12]. Theoretically, the effect of electric fields on membrane tension has been investigated in Ref. [13], which was extended to bending rigidity in Refs [14][15][16][17][18]. When placed in an electric field E, charges of opposite sign will accumulate at both sides of a membrane which can be seen as a capacitor with surface charge densities Σ ± (see Fig.1.A), allowing to calculate the normal component of the electromagnetic stress Σ 2 + − Σ 2 − /ǫ m [19]. For a flat membrane, a direct consequence is electrostriction: at equilibrium, the elastic response of the membrane (Young modulus ∼ 10 7 − 10 8 Pa [5,20]) bal- * Present address: Max Planck Institute for Dynamics and SelfOrganization (MPIDS), Göttingen 37077, Germany † thierry.charitat@ics-cnrs.unistra.fr ances the electrostatic pressure [21]. Beyond this simple effect, membrane fluctuations modify the boundary conditions for the electric field, leading to a subtle coupling between electrostatics and membrane elasticity. Due to membrane finite thickness d m , a bending deformation induces surface element variations of opposite sign on both interface leading to a net ...

Synchrotron Scattering Methods for Nanomaterials and Soft Matter Research

“…High-energy X-rays permit an extension of the conventional Langmuir techniques to study bulk liquid-liquid interfaces and therefore biologically relevant structures formed at these interfaces. For example, an investigation of the alternating electric-field effect on supported lipid membranes by GISAXS revealed a strong decrease in the membrane tension (up to 1 mN/m) and a large increase in membrane rigidity (up to 300 k B T) for local electric potentials of the order of 1 V [169]. These results were quantitatively interpreted in terms of the amplification of membrane surface charge fluctuations resulting in lower tension and increased interaction between charges in the electric double layer leading to the increase of bending rigidity [169].…”

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