Spatial and energetic-entropic decomposition of surface tension in lipid bilayers from molecular dynamics simulations

Abstract

The spatial and groupwise distribution of surface tension in a fully hydrated 256 lipid dipalmitoylphosphatidylcholine (DPPC) bilayer is determined from a 5 ns molecular dynamics simulation by resolving the normal and lateral pressures in space through the introduction of a local virial. The resulting surface tension is separated into contributions from different types of interactions and pairwise terms between lipid headgroups, chains and water. By additionally performing a series of five simulations at constant areas ranging from 0.605 to 0.665 nm2 (each of 6 ns length), it is possible to independently resolve the energetic contributions to surface tension from the area dependence of the interaction energies. This also enables us to calculate the remaining entropic part of the tension and the thermal expansivity. Together with the total lateral pressures this yields a full decomposition of surface tension into energetic and entropic contributions from electrostatics, Lennard-Jones and bonded interactions between lipid chains, headgroups and water molecules. The resulting total surface tension in the bilayer is found to be a sum of very large terms of opposing signs, explaining the sensitivity of simulation surface tension to details in force fields. Headgroup and headgroup–water interactions are identified as attractive on average while the chain region wants to expand the bilayer. Both effects are dominated by entropic contributions but there are also substantial energetic terms in the hydrophobic core. The net lateral pressure is small and relatively smooth compared to the individual components, in agreement with experimental observations of DPPC lipids forming stable bilayers.