Hidden dynamics in rapid changes of bilayer shape

In the past, mechanical models for lipid bilayers have been conceptualized on the basis that the membrane is a ‘unit’ structure where energy is coupled to deformation through single fields for surface curvature and density — valid only for chemically bonded layers. By comparison, real bilayers are composed of two weakly adherent monolayers that can move slowly past one another with negligible input of local energy if shape remains constant. However, when bilayer shape changes rapidly, an unexpected viscous impedance arises from relative motion between layers, which significantly augments conventional retardation by dissipation in hydrodynamic flow. The added dissipation is produced by drag at the monolayer-monolayer interface. This leads to ‘hidden dynamic coupling’ of the layers through density differences that spread diffusively over the surface with long range consequences. Here, we examine the origins of mechanical coupling between layers in bilayers and show that evolution of the differential density between layers creates new dynamics previously overlooked in membrane behavior. To demonstrate the profound affect of dynamic coupling in bilayers, we describe a model situation (supported by experimental evidence) where a nanoscale tube of membrane is pulled rapidly from a macroscopic-size vesicle. Rapid extraction of bilayer through this 1000-fold increase in curvature creates an enormous relative motion between layers near the vesicle-tube junction (molecules in opposite layers slip past at rates approaching 105/s) and, in turn, interlayer drag that dominates the extraction force.