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

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 p...

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Main Authors: Tianyuan Shi, Qiuxia Wei, Zhen Wang, Gong Zhang, Xuesong Sun, Qing-Yu He
Format: Article
Language:English
Published: American Society for Microbiology 2019-05-01
Series:mSphere
Subjects:
Online Access:https://doi.org/10.1128/mSphere.00175-19
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spelling doaj-31c066ff20da437995db06b22d319a822020-11-25T00:27:50ZengAmerican Society for MicrobiologymSphere2379-50422019-05-0143e00175-1910.1128/mSphere.00175-19Photocatalytic Protein Damage by Silver Nanoparticles Circumvents Bacterial Stress Response and Multidrug ResistanceTianyuan ShiQiuxia WeiZhen WangGong ZhangXuesong SunQing-Yu HeAlthough 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.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.https://doi.org/10.1128/mSphere.00175-19silver nanoparticlesantibiotic resistanceiTRAQlightprotein aggregation
collection DOAJ
language English
format Article
sources DOAJ
author Tianyuan Shi
Qiuxia Wei
Zhen Wang
Gong Zhang
Xuesong Sun
Qing-Yu He
spellingShingle 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
mSphere
silver nanoparticles
antibiotic resistance
iTRAQ
light
protein aggregation
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
series mSphere
issn 2379-5042
publishDate 2019-05-01
description 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.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.
topic silver nanoparticles
antibiotic resistance
iTRAQ
light
protein aggregation
url https://doi.org/10.1128/mSphere.00175-19
work_keys_str_mv AT tianyuanshi photocatalyticproteindamagebysilvernanoparticlescircumventsbacterialstressresponseandmultidrugresistance
AT qiuxiawei photocatalyticproteindamagebysilvernanoparticlescircumventsbacterialstressresponseandmultidrugresistance
AT zhenwang photocatalyticproteindamagebysilvernanoparticlescircumventsbacterialstressresponseandmultidrugresistance
AT gongzhang photocatalyticproteindamagebysilvernanoparticlescircumventsbacterialstressresponseandmultidrugresistance
AT xuesongsun photocatalyticproteindamagebysilvernanoparticlescircumventsbacterialstressresponseandmultidrugresistance
AT qingyuhe photocatalyticproteindamagebysilvernanoparticlescircumventsbacterialstressresponseandmultidrugresistance
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