Collective lipid dynamics in biomembranes

Cellular lipids are wonders of biomolecular self-organization whose structure and dynamics are intimately connected with their functionality. Here we review the development and use of NMR spectroscopy in the study of lipid membranes. For liquid-crystalline bilayers, the structure is described by orientational order parameters, while the dynamics entail fluctuations about the mean geometry. Addressing the information gap between molecular structure, dynamics, and function involves magnetic resonance spectroscopy combined with X-ray and neutron scattering approaches. Cholesterol gives a crucial test in liquid-ordered (l_o) membranes, where the bending rigidity oppositely affects solid-state NMR observables-the order parameters increase yet the relaxation rates decrease. By contrast, nonionic surfactants in the liquid-disordered (l_d) state soften the bilayer and decrease the order parameters, thereby enhancing the spin relaxation. This enigma is explained by a model-free power-law that combines the mean-squared amplitudes and fluctuation rates. Collective modes appear on the mesoscale of the bilayer thickness and less, indicating how membrane elasticity emerges from atomistic-level interactions that drive the response to external forces. The unified power-law scaling shows how the bilayer fluidity corresponds to a hydrocarbon liquid of similar chain length. Magnetic resonance spectroscopy thus yields insights into properties that underlie bilayer phase transitions, curvature, and protein-lipid interactions.