Mesoscopic Dynamics in Phospholipid Membranes under Osmotic Stress

Abstract

Phospholipid membranes are biological liquid crystals exhibiting long-range molecular order [1]. Intermolecular interactions at mesoscopic length scales are key for explaining lipid-protein interactions and biomembrane functioning. Elastic deformations in such materials are manifested as director fluctuations with timescales spanning picoseconds to seconds [2]. Here we examine effects of osmotic stress on liquid-crystalline properties of lipid membranes using NMR relaxation methods. Membrane osmotic stress was monitored by addition of osmolytes and gravimetric dehydration. Solid-state 2H longitudinal (R1Z) and transverse quadrupolar-echo decay (R2QE) rates were measured for acyl-chain-perdeuterated lipid multilamellar dispersions. Plots of R1Z rates versus squared segmental order parameters (SCD2) follow an empirical linear function (square-law) suggesting the emergence of 3-D director fluctuations [2]. Slopes of these plots are sensitive to osmotic stress and invariant under temperature variation. Linear trends were also observed for R2QE rates but limited to segments deeper in the bilayer. Enhanced R2QE rates and their temperature dependence indicate additional relaxation contributions from slower dynamics. The dependence of R2QEon SCD2 near the headgroup suggests the onset of 2-D surface undulations. Membrane composition at the transition of 3-D to 2-D collective fluctuations has important implications for biomembrane functioning. The observed slow dynamics are due to mesoscopic phenomena that explain bulk material properties, where the connection between mechanical properties and NMR relaxation involves the fluctuation dissipation theorem. Restricted water accessibility into bilayer may suppress slow dynamic modes at high osmotic stress. Analogous studies with cholesterol in raft-like lipid mixtures [3] report on membrane compositions relevant for biomembrane function. Osmotic stress-mediated lipid dynamics thus opens a new window to exploring their coupling to biomembrane function. [1] T.R. Molugu et al. (2017) Chem. Rev. 117, 12087. [2] Leftin, A. et al. (2011) BBA 1808, 818. [3] T.R. Molugu et al. (2016) Chem. Phys. Lipids 199, 39.