Additional contributions to elastic energy of lipid membranes: Tilt-curvature coupling and curvature gradient

Abstract

Lipid bilayer membranes are flexible thin laterally fluid films consisting of two unimolecular layers of lipids. On spatial scales much larger than the bilayer thickness, the membrane elasticity is well determined by its shape and adequately described by the classical Helfrich Hamiltonian. However, various local membrane heterogeneities can result in a lipids tilt relative to the membrane surface normal. On the basis of the classical elasticity theory of 3D bodies, Hamm and Kozlov [Eur. Phys. J. E 3, 323 (2000)] derived the most general energy functional, taking into account the tilt and bending. Recently, Terzi and Deserno [J. Chem. Phys. 147, 084702 (2017)] showed that Hamm and Kozlov's derivation was incomplete because the tilt-curvature coupling term had been missed. However, the energy functional derived by Terzi and Deserno appeared to be unstable, thereby being invalid for applications. Here, we derive a stable elastic energy functional, showing that the squared gradient of the curvature was missed in both of these works. This change in the energy functional arises from a more accurate consideration of the transverse shear deformation terms and their influence on the membrane stability. We also consider the influence of the prestress terms on the stability of the energy functional, and we show that the effective Gaussian curvature should be neglected because of the stability requirements. We further generalize the theory, including the stretching-compressing deformation modes, and we provide the geometrical interpretation of the terms that were previously missed by Hamm and Kozlov. The physical consequences of the new terms are analyzed in the case of a membrane-mediated interaction of two amphipathic peptides located in the same monolayer. We also provide the expression for director fluctuations, comparing it with that obtained by Terzi and Deserno.