Desiccation resistance and viscoelasticity in model membrane systems

Abstract

Lipid membranes are a basic structural element of all cells. They provide a framework for the physical organization of the cell, act as a scaffold for numerous proteins, and serve as the host site for countless chemical reactions integral to cell function. Several key problems in membrane biophysics hinge on reliable methods for measuring membrane material properties. Properties such as rigidity, fluidity, charge density, etc., are important factors that govern membrane structure and function. As such, we need controllable, reliable, and quantitative methods of probing membrane material properties. In pursuit of such methods, we completed two related projects that, while distinct, aimed to create and apply quantitative measures of membrane material properties to current problems in biophysics.

The first of these two lines of inquiry centered on the pervasive, pathogenic family of mycobacteria that is known to not only cause several diseases but also to survive prolonged periods of dehydration. We developed an experimental model system that mimics the structure of the mycobacterial envelope consisting of an immobile hydrophobic layer supporting a two-dimensionally fluid, glycolipid-rich outer monolayer. With this system, we show that glycolipid containing monolayers, in great contrast to phospholipid monolayers, survive desiccation with no loss of integrity, as assessed by both fluidity and protein binding, revealing a possible cause of mycobacterial persistence.

In the second line of inquiry, we developed another general platform for probing membrane material properties that has produced the first reported observations of viscoelasticity in lipid membranes. We utilized recently developed microrheological techniques on freestanding lipid bilayer systems using high speed video particle tracking. The complex shear modulus of the bilayers was extracted at a variety of temperatures that span the liquid-ordered to disordered phase transition of the membranes. At many temperatures measured, the membranes displayed viscoelastic behavior reminiscent of a Maxwell material, namely elastic at high frequencies and viscous at low frequencies. Moreover, the viscoelastic behavior was suppressed at the critical phase transition temperature where the membranes behave as a purely viscous fluid. Surprisingly, the viscoelastic behavior was found in all of several distinct membrane compositions that were examined.