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Bicelles of various lipid/detergent ratios are commonly used in nuclear magnetic resonance (NMR) studies of membrane-associated molecules without the need to freeze the sample. While a decrease in the size (defined at a low temperature or by the q value) of a bicelle decreases its overall order parameter, the variation of lipid dynamics with a change in the lipid/detergent ratio is unknown. In this study, we report a thorough atomistic level analysis on the variation of lipid dynamics with the size and hydration level of bicelles composed of a phospholipid, 1,2-dimyristoyl-sn-glycero-3-phosphocholine (DMPC), and a detergent, 1,2-dihexanoyl-sn-glycero-3-phosphocholine (DHPC). Two-dimensional (2D) separated-local-field NMR experiments were performed on magnetically aligned bicelles to measure (1)H-(13)C dipolar couplings, which were used to determine order parameters at various (head-group, glycerol, and acyl chain) regions of lipids in the bilayer. From our analysis, we uncover the extreme sensitivity of the glycerol region to the motion of the bicelle, which can be attributed to the effect of viscosity because of an extensive network of hydrogen bonds. As such, the water-membrane interface region exhibits the highest order parameter values among all three regions of a lipid molecule. Our experimental results demonstrate that the laboratory-frame 2D proton-detected-local-field pulse sequence is well-suited for the accurate measurement of motionally averaged (or long-range) weak and multiple (1)H-(13)C dipolar couplings associated with a single carbon site at the natural abundance of (13)C nuclei.

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Comprehensive Analysis of Lipid Dynamics Variation with Lipid Composition and Hydration of Bicelles Using Nuclear Magnetic Resonance (NMR) Spectroscopy