Antibacterial action of nanoparticles by lethal stretching of bacterial cell membranes

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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ORCID for Paul Stoodley: orcid.org/0000-0001-6069-273X

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