X-ray scattering and solid-state deuterium nuclear magnetic resonance probes of structural fluctuations in lipid membranes.

Molecular fluctuations are a dominant feature of biomembranes. Cellular functions might rely on these properties in ways yet to be determined. This expectation is suggested by the fact that membrane deformation and rigidity, which govern molecular fluctuations, have been implicated in a number of cellular functions. However, fluctuations are more challenging to measure than average structures, which partially explain the small number of dedicated studies. Here, it is shown that two accessible laboratory methods, small-angle X-ray scattering and solid-state deuterium nuclear magnetic resonance (NMR), can be used as complementary probes of structural fluctuations in lipid membranes. In the case of X-ray scattering, membrane undulations give rise to logarithmically varying positional correlations that generate scattering peaks with long (power-law) tails. In the case of 2H NMR spectroscopy, fluctuations in the magnetic-coupling energies resulting from molecular motions cause relaxation among the various spin energy levels, and yield a powerful probe of orientational fluctuations of the lipid molecules. A unified interpretation of the combined scattering and 2H NMR data is provided by a liquid-crystalline membrane deformation model. The importance of this approach is that it is possible to utilize a microscopic model for positional and orientational observables to calculate bulk material properties of liquid-crystalline systems.