Punching Membranes: How Lipid Bilayers Withstand and Propagate Mechanical Load

Abstract

Mechanical perturbations are ubiquitous in living cells and many biological functions are strongly dependent on the mechanical response of lipid membranes. We asked how lipid bilayers withstand and also propagate high mechanical load using large-scale atomistic and coarse-grained Molecular Dynamics simulations. We perforated stacked lipid bilayers using a spherical indenter, closely mimicking novel force spectroscopy techniques that capture the fracture of individual membranes, while avoiding substrate effects by probing stacks of model bilayers. We observe a step-wise fracture of individual bilayers in close agreement with experiments. Dwell times of the physiologically more relevant free standing bilayers are lower than those of stacked bilayers. Interestingly, the rupture mechanism as well as the dwell time distribution depend on the nature of the indenter: Only a hydrophilic intender yields the expected log-normal distribution by inducing a pore-growth mechanism. Upon subjecting the bilayer to a longitudinal rather than a perpendicular perturbation, we observe the propagation of a mechanical pulse through the lipid bilayer with the experimentally known speed of sound of ∼1 km/s, again in both atomistic and coarse-grained systems. The computed dispersion follows proposed continuum visco-elastic models and is remarkably low, allowing stress propagation over tens of nanometers before damping Our results provide a better understanding of membrane nanomechanics and indicate that membranes play a role as efficient wave guides for signalling through the cell.