Antibacterial Action of Nanoparticles by Lethal Stretching of Bacterial Cell Membranes
It is commonly accepted that nanoparticles (NPs) can kill bacteria; however, the mechanism of antimicrobial action remains obscure for large NPs that cannot translocate the bacterial cell wall. It is demonstrated that the increase in membrane tension caused by the adsorption of NPs is responsible fo...
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Published in | Advanced materials (Weinheim) Vol. 32; no. 52; pp. e2005679 - n/a |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Germany
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01.12.2020
Wiley-VCH Verlag |
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Abstract | It is commonly accepted that nanoparticles (NPs) can kill bacteria; however, the mechanism of antimicrobial action remains obscure for large NPs that cannot translocate the bacterial cell wall. It is demonstrated that the increase in membrane tension caused by the adsorption of NPs is responsible for mechanical deformation, leading to cell rupture and death. A biophysical model of the NP–membrane interactions is presented which suggests that adsorbed NPs cause membrane stretching and squeezing. This general phenomenon is demonstrated experimentally using both model membranes and Pseudomonas aeruginosa and Staphylococcus aureus, representing Gram‐positive and Gram‐negative bacteria. Hydrophilic and hydrophobic quasi‐spherical and star‐shaped gold (Au)NPs are synthesized to explore the antibacterial mechanism of non‐translocating AuNPs. Direct observation of nanoparticle‐induced membrane tension and squeezing is demonstrated using a custom‐designed microfluidic device, which relieves contraction of the model membrane surface area and eventual lipid bilayer collapse. Quasi‐spherical nanoparticles exhibit a greater bactericidal action due to a higher interactive affinity, resulting in greater membrane stretching and rupturing, corroborating the theoretical model. Electron microscopy techniques are used to characterize the NP–bacterial‐membrane interactions. This combination of experimental and theoretical results confirm the proposed mechanism of membrane‐tension‐induced (mechanical) killing of bacterial cells by non‐translocating NPs.
The mechanism of antimicrobial action for nanoparticles that are unable to translocate across the bacterial cell wall remains obscure. In this work, it is demonstrated that the increase of membrane tension provoked by the adsorption of nanoparticles is responsible for mechanical deformation of the membrane, which leads to bacterial cell rupture and death. |
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AbstractList | It is commonly accepted that nanoparticles (NPs) can kill bacteria; however, the mechanism of antimicrobial action remains obscure for large NPs that cannot translocate the bacterial cell wall. It is demonstrated that the increase in membrane tension caused by the adsorption of NPs is responsible for mechanical deformation, leading to cell rupture and death. A biophysical model of the NP-membrane interactions is presented which suggests that adsorbed NPs cause membrane stretching and squeezing. This general phenomenon is demonstrated experimentally using both model membranes and Pseudomonas aeruginosa and Staphylococcus aureus, representing Gram-positive and Gram-negative bacteria. Hydrophilic and hydrophobic quasi-spherical and star-shaped gold (Au)NPs are synthesized to explore the antibacterial mechanism of non-translocating AuNPs. Direct observation of nanoparticle-induced membrane tension and squeezing is demonstrated using a custom-designed microfluidic device, which relieves contraction of the model membrane surface area and eventual lipid bilayer collapse. Quasi-spherical nanoparticles exhibit a greater bactericidal action due to a higher interactive affinity, resulting in greater membrane stretching and rupturing, corroborating the theoretical model. Electron microscopy techniques are used to characterize the NP-bacterial-membrane interactions. This combination of experimental and theoretical results confirm the proposed mechanism of membrane-tension-induced (mechanical) killing of bacterial cells by non-translocating NPs.It is commonly accepted that nanoparticles (NPs) can kill bacteria; however, the mechanism of antimicrobial action remains obscure for large NPs that cannot translocate the bacterial cell wall. It is demonstrated that the increase in membrane tension caused by the adsorption of NPs is responsible for mechanical deformation, leading to cell rupture and death. A biophysical model of the NP-membrane interactions is presented which suggests that adsorbed NPs cause membrane stretching and squeezing. This general phenomenon is demonstrated experimentally using both model membranes and Pseudomonas aeruginosa and Staphylococcus aureus, representing Gram-positive and Gram-negative bacteria. Hydrophilic and hydrophobic quasi-spherical and star-shaped gold (Au)NPs are synthesized to explore the antibacterial mechanism of non-translocating AuNPs. Direct observation of nanoparticle-induced membrane tension and squeezing is demonstrated using a custom-designed microfluidic device, which relieves contraction of the model membrane surface area and eventual lipid bilayer collapse. Quasi-spherical nanoparticles exhibit a greater bactericidal action due to a higher interactive affinity, resulting in greater membrane stretching and rupturing, corroborating the theoretical model. Electron microscopy techniques are used to characterize the NP-bacterial-membrane interactions. This combination of experimental and theoretical results confirm the proposed mechanism of membrane-tension-induced (mechanical) killing of bacterial cells by non-translocating NPs. It is commonly accepted that nanoparticles (NPs) can kill bacteria; however, the mechanism of antimicrobial action remains obscure for large NPs that cannot translocate the bacterial cell wall. It is demonstrated that the increase in membrane tension caused by the adsorption of NPs is responsible for mechanical deformation, leading to cell rupture and death. A biophysical model of the NP–membrane interactions is presented which suggests that adsorbed NPs cause membrane stretching and squeezing. This general phenomenon is demonstrated experimentally using both model membranes and Pseudomonas aeruginosa and Staphylococcus aureus, representing Gram‐positive and Gram‐negative bacteria. Hydrophilic and hydrophobic quasi‐spherical and star‐shaped gold (Au)NPs are synthesized to explore the antibacterial mechanism of non‐translocating AuNPs. Direct observation of nanoparticle‐induced membrane tension and squeezing is demonstrated using a custom‐designed microfluidic device, which relieves contraction of the model membrane surface area and eventual lipid bilayer collapse. Quasi‐spherical nanoparticles exhibit a greater bactericidal action due to a higher interactive affinity, resulting in greater membrane stretching and rupturing, corroborating the theoretical model. Electron microscopy techniques are used to characterize the NP–bacterial‐membrane interactions. This combination of experimental and theoretical results confirm the proposed mechanism of membrane‐tension‐induced (mechanical) killing of bacterial cells by non‐translocating NPs. It is commonly accepted that nanoparticles (NPs) can kill bacteria; however, the mechanism of antimicrobial action remains obscure for large NPs that cannot translocate the bacterial cell wall. It is demonstrated that the increase in membrane tension caused by the adsorption of NPs is responsible for mechanical deformation, leading to cell rupture and death. A biophysical model of the NP–membrane interactions is presented which suggests that adsorbed NPs cause membrane stretching and squeezing. This general phenomenon is demonstrated experimentally using both model membranes and Pseudomonas aeruginosa and Staphylococcus aureus, representing Gram‐positive and Gram‐negative bacteria. Hydrophilic and hydrophobic quasi‐spherical and star‐shaped gold (Au)NPs are synthesized to explore the antibacterial mechanism of non‐translocating AuNPs. Direct observation of nanoparticle‐induced membrane tension and squeezing is demonstrated using a custom‐designed microfluidic device, which relieves contraction of the model membrane surface area and eventual lipid bilayer collapse. Quasi‐spherical nanoparticles exhibit a greater bactericidal action due to a higher interactive affinity, resulting in greater membrane stretching and rupturing, corroborating the theoretical model. Electron microscopy techniques are used to characterize the NP–bacterial‐membrane interactions. This combination of experimental and theoretical results confirm the proposed mechanism of membrane‐tension‐induced (mechanical) killing of bacterial cells by non‐translocating NPs. The mechanism of antimicrobial action for nanoparticles that are unable to translocate across the bacterial cell wall remains obscure. In this work, it is demonstrated that the increase of membrane tension provoked by the adsorption of nanoparticles is responsible for mechanical deformation of the membrane, which leads to bacterial cell rupture and death. Abstract It is commonly accepted that nanoparticles (NPs) can kill bacteria; however, the mechanism of antimicrobial action remains obscure for large NPs that cannot translocate the bacterial cell wall. It is demonstrated that the increase in membrane tension caused by the adsorption of NPs is responsible for mechanical deformation, leading to cell rupture and death. A biophysical model of the NP–membrane interactions is presented which suggests that adsorbed NPs cause membrane stretching and squeezing. This general phenomenon is demonstrated experimentally using both model membranes and Pseudomonas aeruginosa and Staphylococcus aureus , representing Gram‐positive and Gram‐negative bacteria. Hydrophilic and hydrophobic quasi‐spherical and star‐shaped gold (Au)NPs are synthesized to explore the antibacterial mechanism of non‐translocating AuNPs. Direct observation of nanoparticle‐induced membrane tension and squeezing is demonstrated using a custom‐designed microfluidic device, which relieves contraction of the model membrane surface area and eventual lipid bilayer collapse. Quasi‐spherical nanoparticles exhibit a greater bactericidal action due to a higher interactive affinity, resulting in greater membrane stretching and rupturing, corroborating the theoretical model. Electron microscopy techniques are used to characterize the NP–bacterial‐membrane interactions. This combination of experimental and theoretical results confirm the proposed mechanism of membrane‐tension‐induced (mechanical) killing of bacterial cells by non‐translocating NPs. |
Author | Fleury, Jean‐Baptiste Crawford, Russell J. Nguyen, The Hong Phong Le Guével, Xavier Stoodley, Paul Bryant, Gary Linklater, Denver P. Juodkazis, Saulius Ivanova, Elena P. Baulin, Vladimir A. Hanssen, Eric |
Author_xml | – sequence: 1 givenname: Denver P. surname: Linklater fullname: Linklater, Denver P. organization: Swinburne University of Technology – sequence: 2 givenname: Vladimir A. orcidid: 0000-0003-2086-4271 surname: Baulin fullname: Baulin, Vladimir A. organization: Universitat Rovira i Virgili – sequence: 3 givenname: Xavier surname: Le Guével fullname: Le Guével, Xavier organization: University Grenoble‐Alpes – sequence: 4 givenname: Jean‐Baptiste orcidid: 0000-0003-1878-0108 surname: Fleury fullname: Fleury, Jean‐Baptiste organization: Saarland University – sequence: 5 givenname: Eric orcidid: 0000-0002-8897-4373 surname: Hanssen fullname: Hanssen, Eric organization: University of Melbourne – sequence: 6 givenname: The Hong Phong surname: Nguyen fullname: Nguyen, The Hong Phong organization: Ton Duc Thang University – sequence: 7 givenname: Saulius orcidid: 0000-0003-3542-3874 surname: Juodkazis fullname: Juodkazis, Saulius organization: Swinburne University of Technology – sequence: 8 givenname: Gary surname: Bryant fullname: Bryant, Gary organization: RMIT University – sequence: 9 givenname: Russell J. surname: Crawford fullname: Crawford, Russell J. organization: RMIT University – sequence: 10 givenname: Paul surname: Stoodley fullname: Stoodley, Paul organization: University of Southampton – sequence: 11 givenname: Elena P. orcidid: 0000-0002-5509-8071 surname: Ivanova fullname: Ivanova, Elena P. email: elena.ivanova@rmit.edu.au organization: RMIT University |
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Snippet | It is commonly accepted that nanoparticles (NPs) can kill bacteria; however, the mechanism of antimicrobial action remains obscure for large NPs that cannot... Abstract It is commonly accepted that nanoparticles (NPs) can kill bacteria; however, the mechanism of antimicrobial action remains obscure for large NPs that... |
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SubjectTerms | Anti-Bacterial Agents - chemistry Anti-Bacterial Agents - pharmacology Antiinfectives and antibacterials Bacteria Bacteriology Biological Physics Cell Membrane - chemistry Cell Membrane - drug effects Cell Membrane - metabolism Cell membranes Chemical Sciences Compressing Gold - chemistry Hydrophobic and Hydrophilic Interactions Life Sciences Lipid Bilayers - chemistry Lipid Bilayers - metabolism Lipids Materials science mechano‐bactericidal activity Medicinal Chemistry Metal Nanoparticles - chemistry Microbiology and Parasitology Microfluidic devices Nanoparticles nanotoxicity Physics Pseudomonas aeruginosa Pseudomonas aeruginosa - drug effects Staphylococcus aureus - drug effects Stretching |
Title | Antibacterial Action of Nanoparticles by Lethal Stretching of Bacterial Cell Membranes |
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