Photocatalytic Protein Damage by Silver Nanoparticles Circumvents Bacterial Stress Response and Multidrug Resistance

ABSTRACT Silver nanoparticles (AgNPs) are known for their broad-spectrum antibacterial properties, especially against antibiotic-resistant bacteria. However, the bactericidal mechanism of AgNPs remains unclear. In this study, we found that the bactericidal ability of AgNPs is induced by light. In co...

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Autores principales:	Tianyuan Shi, Qiuxia Wei, Zhen Wang, Gong Zhang, Xuesong Sun, Qing-Yu He
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	silver nanoparticles antibiotic resistance iTRAQ light protein aggregation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/253b3a295b3c40e3823f3ab2e95ac44d
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spelling	oai:doaj.org-article:253b3a295b3c40e3823f3ab2e95ac44d2021-11-15T15:22:20ZPhotocatalytic Protein Damage by Silver Nanoparticles Circumvents Bacterial Stress Response and Multidrug Resistance10.1128/mSphere.00175-192379-5042https://doaj.org/article/253b3a295b3c40e3823f3ab2e95ac44d2019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00175-19https://doaj.org/toc/2379-5042ABSTRACT Silver nanoparticles (AgNPs) are known for their broad-spectrum antibacterial properties, especially against antibiotic-resistant bacteria. However, the bactericidal mechanism of AgNPs remains unclear. In this study, we found that the bactericidal ability of AgNPs is induced by light. In contrast to previous postulates, visible light is unable to trigger silver ion release from AgNPs or to promote AgNPs to induce reactive oxygen species (ROS) in Escherichia coli. In fact, we revealed that light excited AgNPs to induce protein aggregation in a concentration-dependent manner in E. coli, indicating that the bactericidal ability of AgNPs relies on the light-catalyzed oxidation of cellular proteins via direct binding to proteins, which was verified by fluorescence spectra. AgNPs likely absorb the light energy and transfer it to the proteins, leading to the oxidation of proteins and thus promoting the death of the bacteria. Isobaric tags for relative and absolute quantitation (iTRAQ)-based proteomics revealed that the bacteria failed to develop effective resistance to the light-excited AgNPs. This direct physical mechanism is unlikely to be counteracted by any known drug resistance mechanisms of bacteria and therefore may serve as a last resort against drug resistance. This mechanism also provides a practical hint regarding the antimicrobial application of AgNPs—light exposure improves the efficacy of AgNPs. IMPORTANCE Although silver nanoparticles (AgNPs) are well known for their antibacterial properties, the mechanism by which they kill bacterial cells remains a topic of debate. In this study, we uncovered the bactericidal mechanism of AgNPs, which is induced by light. We tested the efficacy of AgNPs against a panel of antimicrobial-resistant pathogens as well as Escherichia coli under conditions of light and darkness and revealed that light excited the AgNPs to promote protein aggregation within the bacterial cells. Our report makes a significant contribution to the literature because this mechanism bypasses microbial drug resistance mechanisms, thus presenting a viable option for the treatment of multidrug-resistant bacteria.Tianyuan ShiQiuxia WeiZhen WangGong ZhangXuesong SunQing-Yu HeAmerican Society for Microbiologyarticlesilver nanoparticlesantibiotic resistanceiTRAQlightprotein aggregationMicrobiologyQR1-502ENmSphere, Vol 4, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	silver nanoparticles antibiotic resistance iTRAQ light protein aggregation Microbiology QR1-502
spellingShingle	silver nanoparticles antibiotic resistance iTRAQ light protein aggregation Microbiology QR1-502 Tianyuan Shi Qiuxia Wei Zhen Wang Gong Zhang Xuesong Sun Qing-Yu He Photocatalytic Protein Damage by Silver Nanoparticles Circumvents Bacterial Stress Response and Multidrug Resistance
description	ABSTRACT Silver nanoparticles (AgNPs) are known for their broad-spectrum antibacterial properties, especially against antibiotic-resistant bacteria. However, the bactericidal mechanism of AgNPs remains unclear. In this study, we found that the bactericidal ability of AgNPs is induced by light. In contrast to previous postulates, visible light is unable to trigger silver ion release from AgNPs or to promote AgNPs to induce reactive oxygen species (ROS) in Escherichia coli. In fact, we revealed that light excited AgNPs to induce protein aggregation in a concentration-dependent manner in E. coli, indicating that the bactericidal ability of AgNPs relies on the light-catalyzed oxidation of cellular proteins via direct binding to proteins, which was verified by fluorescence spectra. AgNPs likely absorb the light energy and transfer it to the proteins, leading to the oxidation of proteins and thus promoting the death of the bacteria. Isobaric tags for relative and absolute quantitation (iTRAQ)-based proteomics revealed that the bacteria failed to develop effective resistance to the light-excited AgNPs. This direct physical mechanism is unlikely to be counteracted by any known drug resistance mechanisms of bacteria and therefore may serve as a last resort against drug resistance. This mechanism also provides a practical hint regarding the antimicrobial application of AgNPs—light exposure improves the efficacy of AgNPs. IMPORTANCE Although silver nanoparticles (AgNPs) are well known for their antibacterial properties, the mechanism by which they kill bacterial cells remains a topic of debate. In this study, we uncovered the bactericidal mechanism of AgNPs, which is induced by light. We tested the efficacy of AgNPs against a panel of antimicrobial-resistant pathogens as well as Escherichia coli under conditions of light and darkness and revealed that light excited the AgNPs to promote protein aggregation within the bacterial cells. Our report makes a significant contribution to the literature because this mechanism bypasses microbial drug resistance mechanisms, thus presenting a viable option for the treatment of multidrug-resistant bacteria.
format	article
author	Tianyuan Shi Qiuxia Wei Zhen Wang Gong Zhang Xuesong Sun Qing-Yu He
author_facet	Tianyuan Shi Qiuxia Wei Zhen Wang Gong Zhang Xuesong Sun Qing-Yu He
author_sort	Tianyuan Shi
title	Photocatalytic Protein Damage by Silver Nanoparticles Circumvents Bacterial Stress Response and Multidrug Resistance
title_short	Photocatalytic Protein Damage by Silver Nanoparticles Circumvents Bacterial Stress Response and Multidrug Resistance
title_full	Photocatalytic Protein Damage by Silver Nanoparticles Circumvents Bacterial Stress Response and Multidrug Resistance
title_fullStr	Photocatalytic Protein Damage by Silver Nanoparticles Circumvents Bacterial Stress Response and Multidrug Resistance
title_full_unstemmed	Photocatalytic Protein Damage by Silver Nanoparticles Circumvents Bacterial Stress Response and Multidrug Resistance
title_sort	photocatalytic protein damage by silver nanoparticles circumvents bacterial stress response and multidrug resistance
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/253b3a295b3c40e3823f3ab2e95ac44d
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_version_	1718427998784323584

Photocatalytic Protein Damage by Silver Nanoparticles Circumvents Bacterial Stress Response and Multidrug Resistance

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