Emergence of Membrane Material Parameters Revealed by Solid-State 2H NMR Spectroscopy

Abstract

The emergence of the material properties of lipid membranes is a topic of current interest in quantitative biophysics. At the smallest length scale, lipid membranes are collections of atoms whose dynamics can be traced by molecular dynamics simulations. At cellular length scales, they are continuous hydrophobic barriers, which together with membrane proteins regulate trafficking and cell signaling. Somewhere in this broad range, material properties emerge from the ensemble of atoms. How can we understand this emergence behavior? Here we show that solid-state 2H NMR spectroscopy is powerful, because as opposed to typical scattering experiments it provides information over a range of length scales. Specifically, solid-state 2H NMR provides atomistically resolved order parameters and dynamics of flexible phospholipids within the liquid-crystalline bilayer [1]. By measuring the membrane response to osmotic stress we can disentangle how bulk material properties emerge from atomistic-level interactions. Examples include structural parameters such as the area per lipid and the volumetric thickness plus the associated moduli for elastic deformation. Data for samples under osmotic stress allow an insightful analysis of intermembrane interactions by distinguishing between collective undulatory and quasi-elastic contributions at large length scales versus short-range non-collective (molecular) effects. By calculating the area elastic modulus over a substantial range of osmotic pressures, collective bilayer properties are found to emerge over very short length scales, on the order of the bilayer thickness or even less. Notably the emergence of lipid material properties on this length scale determines what model is most appropriate to study lipid-protein interactions [2]. A continuum flexible surface model (FSM) for lipid-protein interactions on the mesoscopic length scale can optimally capture the essential material features that govern biomembrane functions. [1] J.Kinnun et al. (2015) Biochim.Biophys.Acta 1848, 256. [2] M.F.Brown (2017) Annu.Rev.Biophys. 46, 379.