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

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. Finally, 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.

Authors:
 [1];  [1];  [2];  [3];  [4];  [1];  [5];  [1]
  1. Brookhaven National Lab. (BNL), Upton, NY (United States)
  2. Joint Inst. for Nuclear Research (JINR), Dubna (Russian Federation)
  3. Inst. of Nanoscience and Cryogenics, Grenoble (France)
  4. Petersburg Nuclear Physics Inst. Gatchina (Russia)
  5. European Synchrotron Radiation Facility (ESRF), Grenoble (France)
Publication Date:
Research Org.:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); Russian Foundation for Basic Research
OSTI Identifier:
1237168
Alternate Identifier(s):
OSTI ID: 1340385
Report Number(s):
BNL-108276-2015-JA; BNL-112571-2016-JA
Journal ID: ISSN 2041-1723; R&D Project: LS001
Grant/Contract Number:  
SC0012704
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; Membrane biophysics; Membrane lipids; 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Zhernenkov, Mikhail, Bolmatov, Dima, Soloviov, Dmitry, Zhernenkov, Kirill, Toperverg, Boris P., Cunsolo, Alessandro, Bosak, Alexey, and Cai, Yong. Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations. United States: N. p., 2016. Web. doi:10.1038/ncomms11575.
Zhernenkov, Mikhail, Bolmatov, Dima, Soloviov, Dmitry, Zhernenkov, Kirill, Toperverg, Boris P., Cunsolo, Alessandro, Bosak, Alexey, & Cai, Yong. Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations. United States. https://doi.org/10.1038/ncomms11575
Zhernenkov, Mikhail, Bolmatov, Dima, Soloviov, Dmitry, Zhernenkov, Kirill, Toperverg, Boris P., Cunsolo, Alessandro, Bosak, Alexey, and Cai, Yong. Thu . "Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations". United States. https://doi.org/10.1038/ncomms11575. https://www.osti.gov/servlets/purl/1237168.
@article{osti_1237168,
title = {Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations},
author = {Zhernenkov, Mikhail and Bolmatov, Dima and Soloviov, Dmitry and Zhernenkov, Kirill and Toperverg, Boris P. and Cunsolo, Alessandro and Bosak, Alexey and Cai, Yong},
abstractNote = {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. Finally, 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.},
doi = {10.1038/ncomms11575},
journal = {Nature Communications},
number = ,
volume = 7,
place = {United States},
year = {Thu May 12 00:00:00 EDT 2016},
month = {Thu May 12 00:00:00 EDT 2016}
}

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