Hydration-Modulated Collective Dynamics of Membrane Lipids are Revealed by Solid-State 2H NMR Relaxation

Abstract

Investigations of model membranes aim to understand the atomistic interactions that can explain bulk membrane lipid properties in relation to key biological functions [1]. Solid-state 2H nuclear magnetic resonance (NMR) spectroscopy uniquely provides such information by probing structure and dynamics of membranes [2,3]. Here we examine the effect of water on the liquid-crystalline properties of amphiphilic membrane lipids using NMR relaxometry. We performed NMR longitudinal (R1Z), transverse quadrupolar-echo decay (R2QE) and quadrupolar Carr-Purcell-Meiboom-Gill (QCPMG) relaxation (R2CP) experiments on DMPC-d54 bilayers, to study membrane-lipid dynamics over time scales ranging from 10−9s to 10−3s. The plots of R1Z rates versus squared segmental order parameters (SCD2) follow an empirical square-law behavior showing the emergence of collective lipid dynamics [4]. Such a functional behavior characterizes 3-D order-director fluctuations due to the onset of membrane elasticity over atomistic dimensions [4]. The transverse relaxation rates also show similar results at low hydration. Yet at high hydration, a further enhancement versus the functional square-law plot is evident for segments deeper in the bilayers. Additional contributions from slower dynamics involving water-mediated membrane deformation are evident over mesoscopic length scales on the order of bilayer thickness. The slow dynamics at high hydration must be a consequence of modulation of elastic properties of lipid bilayer. Analysis of the QCPMG frequency dispersions as function of hydration and temperature reveals quantitative information on viscoelastic properties of the liquid-crystalline media. Similar studies in the presence of proteins and peptides give insights into optimized lipid hydration for biomembrane function. [1] A. Leftin et al. (2014) BJ. (in press). [2] K. J. Mallikarjuniah et al. (2011) BJ 100 98-107. [3] J. J. Kinnun et al. (2014) BBA (in press). [4] M. F. Brown et al. (2002) JACS 124, 8471-8484.