Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations

Mikhail Zhernenkov (), Dima Bolmatov, Dmitry Soloviov, Kirill Zhernenkov, Boris P. Toperverg, Alessandro Cunsolo, Alexey Bosak and Yong Q. Cai
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Mikhail Zhernenkov: National Synchrotron Light Source II, Brookhaven National Laboratory
Dima Bolmatov: National Synchrotron Light Source II, Brookhaven National Laboratory
Dmitry Soloviov: Frank Laboratory of Neutron Physics, Joint Institute for Nuclear Research
Kirill Zhernenkov: Institut Nanosciences et Cryogénie, Commissariat à l’Energie Atomique
Boris P. Toperverg: Petersburg Nuclear Physics Institute
Alessandro Cunsolo: National Synchrotron Light Source II, Brookhaven National Laboratory
Alexey Bosak: European Synchrotron Radiation Facility
Yong Q. Cai: National Synchrotron Light Source II, Brookhaven National Laboratory

Nature Communications, 2016, vol. 7, issue 1, 1-10

Abstract: 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.

Date: 2016
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DOI: 10.1038/ncomms11575

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