Elastic Deformation and Collective Dynamics in Lipid Membranes: A Solid-State 2H NMR Relaxation Study

Abstract

Biomembrane functioning is significantly influenced by the composition and structure of the liquid-crystalline lipid bilayer [1]. Solid-state 2H NMR spectroscopy provides information about atomistic interactions among the membrane constituents by simultaneously probing structure and dynamics [2]. Here we examine the effect of water, osmolytes, cholesterol, and detergents on the liquid-crystalline properties of lipid membranes using NMR relaxation methods. We performed 2H NMR longitudinal (R1Z) and transverse quadrupolar-echo decay (R2QE) experiments on DMPC-d54 bilayers to study membrane lipid dynamics over the time scale ranging from nanoseconds to milliseconds. Plots of R1Z rates or transverse relaxation rates versus squared segmental order parameters (SCD2) show the emergence of collective lipid dynamics [3]. Such a functional behavior characterizes 3-D order-director fluctuations, due to the onset of membrane elasticity [3]. Yet at high hydration, a further R2QE enhancement and confinement of the functional square-law to the segments deeper in the bilayer is seen. Additional contributions from slower dynamics involving water-mediated membrane deformation are evident over mesoscopic length scales on the order of bilayer thickness. Such structural deformations are also evident from bilayer structural parameters calculated using a statistical mean-torque model [4]. The slow dynamics at high hydration or correspondingly low cholesterol or osmolyte concentration are due to modulation of elastic properties of the lipid bilayer. Analysis of the frequency dispersion of the transverse relaxation as a function of such external parameters reveals viscoelastic properties of the liquid-crystalline membranes. Such studies give insights into lipid rafts and membrane composition relevant for biomembrane function. [1] A. Leftin et al. (2014) Biophys. J. 107, 2274[2] K.J. Mallikarjuniah et al. (2011) Biophys. J.100, 98. [3] A. Leftin et al. (2014) eMagRes 4, 199. [4] J.J. Kinnun et al. (2015) BBA 1848, 246.