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Modulation of host lipid membrane elasticity and dipole potential induced by bacterial membrane vesicles

View ORCID ProfileAshutosh Prince, View ORCID ProfileAnuj Tiwari, Titas Mandal, Kuldeep Sharma, Nikhil Kanik, View ORCID ProfileDeepak Kumar Sinha, View ORCID ProfileMohammed Saleem
doi: https://doi.org/10.1101/827519
Ashutosh Prince
1Department of Life Sciences, National Institute of Technology, Rourkela, India
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Anuj Tiwari
1Department of Life Sciences, National Institute of Technology, Rourkela, India
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Titas Mandal
1Department of Life Sciences, National Institute of Technology, Rourkela, India
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Kuldeep Sharma
1Department of Life Sciences, National Institute of Technology, Rourkela, India
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Nikhil Kanik
1Department of Life Sciences, National Institute of Technology, Rourkela, India
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Deepak Kumar Sinha
2Department of Biological Chemistry, Indian Association for the Cultivation of Sciences, Kolkata, India
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Mohammed Saleem
3School of Biological Sciences, National Institute of Science Education and Research, Bhubaneswar, India
4Homi Bhabha National Institute, Mumbai, India
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  • For correspondence: saleem@niser.ac.in
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Abstract

Bacterial membrane vesicles (MVs) facilitate long-distance delivery of virulence factors crucial for pathogenicity. The entry and trafficking mechanisms of virulence factors inside host cells is recently emerging, however, if bacterial MVs modulate the physicochemical properties of the host lipid membrane remains unknown. Here we reconstitute the interaction of bacterial MV with host cell lipid membranes and quantitatively show that bacterial MV interaction increases the fluidity, dipole potential and elasticity of a biologically relevant multi-component host membrane. The presence of cylindrical lipids such as phosphatidylcholine and phosphatidylinositol and a moderate acyl chain length of C16 helps the MV interaction. While significant binding of bacterial MVs to the raft-like lipid membranes with phase separated regions of the membrane was observed, however, MVs have a preference for binding to the liquid disordered regions of the membrane. Further, the elevated levels of cholesterol tend to hinder the interaction of bacterial MVs. We further quantify the change in excess Gibbs free energy of mixing of bacterial MVs with host lipid membranes driving the modulation of host membrane parameters. The findings may have significant implications on the regulation of host machineries by pathogen through manipulation of host membrane properties.

Significance Statement Bacterial membrane vesicles (MVs) act as the long-distance delivery tools for virulence factor and thus, directly implicated in host-pathogen interactions and pathogenicity. While the mechanisms of virulence transfer is only recently emerging, however, the interaction of MVs the host cell membrane remains largely unexplored. Whether the MVs interaction can locally modulate the host lipid membrane physicochemical properties (such as fluidity, dipole potential and elasticity) remains unknown. Here, we quantitatively investigate the lipid specificity of E. Coli MV interaction and this results in increase in the fluidity, dipole potential and in-plane elasticity of a biologically relevant multi-component host membrane. The findings could be important for numerous cell-signaling processes as well as downstream events involving membrane-membrane fusion during process of phagosome maturation.

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  • Manuscript has been restructured and figures are rearranged.

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Posted February 14, 2020.
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Modulation of host lipid membrane elasticity and dipole potential induced by bacterial membrane vesicles
Ashutosh Prince, Anuj Tiwari, Titas Mandal, Kuldeep Sharma, Nikhil Kanik, Deepak Kumar Sinha, Mohammed Saleem
bioRxiv 827519; doi: https://doi.org/10.1101/827519
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Modulation of host lipid membrane elasticity and dipole potential induced by bacterial membrane vesicles
Ashutosh Prince, Anuj Tiwari, Titas Mandal, Kuldeep Sharma, Nikhil Kanik, Deepak Kumar Sinha, Mohammed Saleem
bioRxiv 827519; doi: https://doi.org/10.1101/827519

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