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Antibacterial action of nanoparticles by lethal stretching of bacterial cell membranes

Antibacterial action of nanoparticles by lethal stretching of bacterial cell membranes
Antibacterial action of nanoparticles by lethal stretching of bacterial cell membranes
It is commonly accepted that nanoparticles can kill bacteria; however, the mechanism of antimicrobial action remains obscure for nanoparticles that are unable to be translocated across the bacterial cell membrane by the passive or active processes that exist for mammalian cells. In this study, we demonstrate that the increase of membrane tension provoked by the adsorption of nanoparticles (NP) is responsible for mechanical deformation of the membrane that leads to cell rupture and consequent bacterial cell death. We present a biophysical model of the NP- membrane interactions. The theoretical model suggests that adsorbed NPs can lead to global stretching and squeezing of the membrane. This general phenomenon was revealed experimentally using both model membranes and bacterial cells. Hydrophilic and hydrophobic quasi-spherical and star shaped gold (Au)NPs were synthesised to explore the antibacterial mechanism of non-translocating AuNPs in vitro. Direct observation of nanoparticle-induced membrane tension and squeezing was realised by a custom-designed microfluidic device that revealed the contraction of the model membrane surface area that resulted in the eventual collapse of the lipid bilayer. Quasi-spherical nanoparticles exhibited a greater bactericidal action due to a higher interactive affinity that resulted in higher degrees of membrane stretching and rupturing, as confirmed by the theoretical model. Electron microscopy techniques were used to characterise the nanoparticle-bacterial-membrane interactions. This combination of experimental and theoretical results confirmed the proposed mechanism of membrane-tension-induced (mechanical) killing of bacterial cells by non-translocating NPs.
Mechano-bactericidal,, nanoparticles
1521-4095
Linklater, Denver P.
687ee114-17b0-4490-a120-f0a95f72a6b7
Baulin, Vladimir A.
c7205990-1ca9-418b-b6ca-8410fb465315
Juodkazis, Saulius
1204b9c5-5339-4e78-af5a-6315a7b399e9
Bryant, G.
e0ef9212-685e-469d-a525-8d9e22097aaa
Crawford, Russell J.
ae5376aa-acf9-4904-bcfa-f1aa259f4aa9
Stoodley, Paul
08614665-92a9-4466-806e-20c6daeb483f
Ivanova, Elena
bbd5a829-75e5-4bed-ae44-5fddd9976470
Linklater, Denver P.
687ee114-17b0-4490-a120-f0a95f72a6b7
Baulin, Vladimir A.
c7205990-1ca9-418b-b6ca-8410fb465315
Juodkazis, Saulius
1204b9c5-5339-4e78-af5a-6315a7b399e9
Bryant, G.
e0ef9212-685e-469d-a525-8d9e22097aaa
Crawford, Russell J.
ae5376aa-acf9-4904-bcfa-f1aa259f4aa9
Stoodley, Paul
08614665-92a9-4466-806e-20c6daeb483f
Ivanova, Elena
bbd5a829-75e5-4bed-ae44-5fddd9976470

Linklater, Denver P., Baulin, Vladimir A., Juodkazis, Saulius, Bryant, G., Crawford, Russell J., Stoodley, Paul and Ivanova, Elena (2020) Antibacterial action of nanoparticles by lethal stretching of bacterial cell membranes. Advanced Materials, 32 (52), [2005679]. (doi:10.1002/adma.202005679).

Record type: Article

Abstract

It is commonly accepted that nanoparticles can kill bacteria; however, the mechanism of antimicrobial action remains obscure for nanoparticles that are unable to be translocated across the bacterial cell membrane by the passive or active processes that exist for mammalian cells. In this study, we demonstrate that the increase of membrane tension provoked by the adsorption of nanoparticles (NP) is responsible for mechanical deformation of the membrane that leads to cell rupture and consequent bacterial cell death. We present a biophysical model of the NP- membrane interactions. The theoretical model suggests that adsorbed NPs can lead to global stretching and squeezing of the membrane. This general phenomenon was revealed experimentally using both model membranes and bacterial cells. Hydrophilic and hydrophobic quasi-spherical and star shaped gold (Au)NPs were synthesised to explore the antibacterial mechanism of non-translocating AuNPs in vitro. Direct observation of nanoparticle-induced membrane tension and squeezing was realised by a custom-designed microfluidic device that revealed the contraction of the model membrane surface area that resulted in the eventual collapse of the lipid bilayer. Quasi-spherical nanoparticles exhibited a greater bactericidal action due to a higher interactive affinity that resulted in higher degrees of membrane stretching and rupturing, as confirmed by the theoretical model. Electron microscopy techniques were used to characterise the nanoparticle-bacterial-membrane interactions. This combination of experimental and theoretical results confirmed the proposed mechanism of membrane-tension-induced (mechanical) killing of bacterial cells by non-translocating NPs.

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Antibacterial action of nanoparticles by lethal stretching of bacterial cell membranes_Advanced Materials_Edited (2) - Accepted Manuscript
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More information

Accepted/In Press date: 7 October 2020
e-pub ahead of print date: 12 November 2020
Published date: 28 December 2020
Keywords: Mechano-bactericidal,, nanoparticles

Identifiers

Local EPrints ID: 444857
URI: http://eprints.soton.ac.uk/id/eprint/444857
ISSN: 1521-4095
PURE UUID: 2d3c5757-d243-4162-bf84-8cf7862f360d
ORCID for Paul Stoodley: ORCID iD orcid.org/0000-0001-6069-273X

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Date deposited: 06 Nov 2020 17:33
Last modified: 28 Apr 2022 05:34

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Contributors

Author: Denver P. Linklater
Author: Vladimir A. Baulin
Author: Saulius Juodkazis
Author: G. Bryant
Author: Russell J. Crawford
Author: Paul Stoodley ORCID iD
Author: Elena Ivanova

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