Abstract
The passive transport of molecules through a cell membrane relies on thermal motions of the lipids. However, the nature of transmembrane transport and the precise mechanism remain elusive and call for a comprehensive study of phonon excitations. Here we report a high resolution inelastic X-ray scattering study of the in-plane phonon excitations in 1,2-dipalmitoyl-sn-glycero-3-phosphocholine above and below the main transition temperature. In the gel phase, for the first time, we observe low-frequency transverse modes, which exhibit a phonon gap when the lipid transitions into the fluid phase. We argue that the phonon gap signifies the formation of short-lived nanometre-scale lipid clusters and transient pores, which facilitate the passive molecular transport across the bilayer plane. Our findings suggest that the phononic motion of the hydrocarbon tails provides an effective mechanism of passive transport, and illustrate the importance of the collective dynamics of biomembranes.
Highlights
The passive transport of molecules through a cell membrane relies on thermal motions of the lipids
It is noteworthy that the dynamics of the fully hydrated DPPC membrane is interesting, since this lipid is a major constituent of the pulmonary surfactant, through which oxygen must penetrate before it can reach the lung tissue[34]
We provide clear evidence for the high-frequency longitudinal phonon modes previously predicted by molecular dynamics simulations in the Lb’ phase[23], and for their apparent softening upon the DPPC lipid transition into the La phase
Summary
The passive transport of molecules through a cell membrane relies on thermal motions of the lipids. Because of their polar head groups and two hydrophobic hydrocarbon tails, lipids spontaneously form bilayers in aqueous environments Such a lipid bilayer provides both a stable enclosure for the cell contents and the fluidity and mobility required for the cell to carry out its functions, including passive transport of molecules needed to support the biological functions. Studying the thermally induced ultra-fast vibrations of DPPC is crucial for understanding the oxygen permeation, in particular, and, more generally, the nature of transmembrane small molecule passive transport[7]. We provide clear evidence for the high-frequency longitudinal phonon modes previously predicted by molecular dynamics simulations in the Lb’ (gel) phase[23], and for their apparent softening upon the DPPC lipid transition into the La (fluid) phase. We discuss and explain the importance of the observed low-frequency phononic band gap in the context of solute diffusion in lipid bilayers, which highlights the crucial role of phonons for the passive transmembrane transport
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