Multiplex antibacterial processes and risk in resistant phenotype by high oxidation-state nanoparticles: New killing process and mechanism investigations

I. Ling Hsu; Fang Hao Yeh; Yu Cheng Chin; Chun In Cheung; Zi Chun Chia; Li Xing Yang; Ya Jyun Chen; Ting Yu Cheng; Shu Pao Wu; Pei Jane Tsai; Nan Yao Lee; Mei Yi Liao; Chih Chia Huang

doi:10.1016/j.cej.2020.128266

Multiplex antibacterial processes and risk in resistant phenotype by high oxidation-state nanoparticles: New killing process and mechanism investigations

I. Ling Hsu, Fang Hao Yeh, Yu Cheng Chin, Chun In Cheung, Zi Chun Chia, Li Xing Yang, Ya Jyun Chen, Ting Yu Cheng, Shu Pao Wu, Pei Jane Tsai, Nan Yao Lee, Mei Yi Liao, Chih Chia Huang

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9 Citations (Scopus)

Abstract

Although inorganic silver-based nanoparticles (NPs) have been used to replace antibiotics to treat environmental microorganisms, the silver ion diffusion mechanism takes at least hours to poison the bacteria and cannot destruct the bacteria immediately. In this paper, we developed a concise oxidation process of heterostructured Ag@AuAg hollow NPs in a H₂O₂/PBS solution to generate AgCl nanocrystals and high-oxidation-state (hos) metal species. The hos/AgCl-assembled NPs offered a strong redox reaction to kill bacteria at 1.25 ppm_[Ag] which was lower minimal inhibition concentration value than the utility of Ag ions and Ag NPs. A rapid meet-dip-kill process to disintegrate the bacterial membrane was observed within 60 min. The continuous release of Ag ions from AgCl blocks served as a smart bactericide to sustainably inhibit bacterial growth up to 7 days. The hos/AgCl-based bactericide induced enhanced evolution of a distinctive subpopulation with rigid membrane structure against both Ag ions and Ag-based NPs. This Ag-resistant persister behaved the downregulation of energy consumption and the physical insulation for Ag ions by secreting bio-reductants to convert Ag ions to less toxic Ag NPs. Based on our findings, hos/AgCl-assembled NPs endowed multiple antibacterial effects with no prominent findings of toxicity in the liver and kidneys, which opens a new era to understand the antimicrobial mechanism and resistant risk of Ag-related NPs for future clinical and environmental application.

Original language	English
Article number	128266
Journal	Chemical Engineering Journal
Volume	409
DOIs	https://doi.org/10.1016/j.cej.2020.128266
Publication status	Published - 2021 Apr 1

All Science Journal Classification (ASJC) codes

Chemistry(all)
Environmental Chemistry
Chemical Engineering(all)
Industrial and Manufacturing Engineering

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10.1016/j.cej.2020.128266

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Hsu, I. L., Yeh, F. H., Chin, Y. C., Cheung, C. I., Chia, Z. C., Yang, L. X., Chen, Y. J., Cheng, T. Y., Wu, S. P., Tsai, P. J., Lee, N. Y., Liao, M. Y., & Huang, C. C. (2021). Multiplex antibacterial processes and risk in resistant phenotype by high oxidation-state nanoparticles: New killing process and mechanism investigations. Chemical Engineering Journal, 409, [128266]. https://doi.org/10.1016/j.cej.2020.128266

@article{97915bb319b442068d2c4538722cc0c5,

title = "Multiplex antibacterial processes and risk in resistant phenotype by high oxidation-state nanoparticles: New killing process and mechanism investigations",

abstract = "Although inorganic silver-based nanoparticles (NPs) have been used to replace antibiotics to treat environmental microorganisms, the silver ion diffusion mechanism takes at least hours to poison the bacteria and cannot destruct the bacteria immediately. In this paper, we developed a concise oxidation process of heterostructured Ag@AuAg hollow NPs in a H2O2/PBS solution to generate AgCl nanocrystals and high-oxidation-state (hos) metal species. The hos/AgCl-assembled NPs offered a strong redox reaction to kill bacteria at 1.25 ppm[Ag] which was lower minimal inhibition concentration value than the utility of Ag ions and Ag NPs. A rapid meet-dip-kill process to disintegrate the bacterial membrane was observed within 60 min. The continuous release of Ag ions from AgCl blocks served as a smart bactericide to sustainably inhibit bacterial growth up to 7 days. The hos/AgCl-based bactericide induced enhanced evolution of a distinctive subpopulation with rigid membrane structure against both Ag ions and Ag-based NPs. This Ag-resistant persister behaved the downregulation of energy consumption and the physical insulation for Ag ions by secreting bio-reductants to convert Ag ions to less toxic Ag NPs. Based on our findings, hos/AgCl-assembled NPs endowed multiple antibacterial effects with no prominent findings of toxicity in the liver and kidneys, which opens a new era to understand the antimicrobial mechanism and resistant risk of Ag-related NPs for future clinical and environmental application.",

author = "Hsu, {I. Ling} and Yeh, {Fang Hao} and Chin, {Yu Cheng} and Cheung, {Chun In} and Chia, {Zi Chun} and Yang, {Li Xing} and Chen, {Ya Jyun} and Cheng, {Ting Yu} and Wu, {Shu Pao} and Tsai, {Pei Jane} and Lee, {Nan Yao} and Liao, {Mei Yi} and Huang, {Chih Chia}",

note = "Funding Information: This work was supported in part by grants from the Ministry of Science and Technology, Taiwan ( MOST 108-2113-M-006 -012-MY3 , MOST 108-2622-M-006-001-CC1 , MOST 109-2113-M-153-001 -, MOST 108-2320-B-006-043-MY3 , MOST 108-2320-B-006-013 -, MOST 109-2327-B-009-001 -, MOST 109-2113-M-153-001 -, MOST 109-2320-B-006-063 , MOST 109-2327-B-006-002 ), and by a grant from the Taipei City Hospital (TCH) and the Department of Health, Taipei City Government (TCH No. 10901-62-001). This work was financially supported by the Center of Applied Nanomedicine, National Cheng Kung University from The Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE) in Taiwan. The authors gratefully acknowledge the use of inductivcly coupled plasma-mass spectrometer (ICP-MS) equipment belonging to the Instrument Center of National Cheng Kung University. Publisher Copyright: {\textcopyright} 2020 Elsevier B.V.",

year = "2021",

month = apr,

day = "1",

doi = "10.1016/j.cej.2020.128266",

language = "English",

volume = "409",

journal = "Chemical Engineering Journal",

issn = "1385-8947",

publisher = "Elsevier",

}

Hsu, IL, Yeh, FH, Chin, YC, Cheung, CI, Chia, ZC, Yang, LX, Chen, YJ, Cheng, TY, Wu, SP, Tsai, PJ , Lee, NY, Liao, MY & Huang, CC 2021, 'Multiplex antibacterial processes and risk in resistant phenotype by high oxidation-state nanoparticles: New killing process and mechanism investigations', Chemical Engineering Journal, vol. 409, 128266. https://doi.org/10.1016/j.cej.2020.128266

TY - JOUR

T1 - Multiplex antibacterial processes and risk in resistant phenotype by high oxidation-state nanoparticles

T2 - New killing process and mechanism investigations

AU - Hsu, I. Ling

AU - Yeh, Fang Hao

AU - Chin, Yu Cheng

AU - Cheung, Chun In

AU - Chia, Zi Chun

AU - Yang, Li Xing

AU - Chen, Ya Jyun

AU - Cheng, Ting Yu

AU - Wu, Shu Pao

AU - Tsai, Pei Jane

AU - Lee, Nan Yao

AU - Liao, Mei Yi

AU - Huang, Chih Chia

N1 - Funding Information: This work was supported in part by grants from the Ministry of Science and Technology, Taiwan ( MOST 108-2113-M-006 -012-MY3 , MOST 108-2622-M-006-001-CC1 , MOST 109-2113-M-153-001 -, MOST 108-2320-B-006-043-MY3 , MOST 108-2320-B-006-013 -, MOST 109-2327-B-009-001 -, MOST 109-2113-M-153-001 -, MOST 109-2320-B-006-063 , MOST 109-2327-B-006-002 ), and by a grant from the Taipei City Hospital (TCH) and the Department of Health, Taipei City Government (TCH No. 10901-62-001). This work was financially supported by the Center of Applied Nanomedicine, National Cheng Kung University from The Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE) in Taiwan. The authors gratefully acknowledge the use of inductivcly coupled plasma-mass spectrometer (ICP-MS) equipment belonging to the Instrument Center of National Cheng Kung University. Publisher Copyright: © 2020 Elsevier B.V.

PY - 2021/4/1

Y1 - 2021/4/1

N2 - Although inorganic silver-based nanoparticles (NPs) have been used to replace antibiotics to treat environmental microorganisms, the silver ion diffusion mechanism takes at least hours to poison the bacteria and cannot destruct the bacteria immediately. In this paper, we developed a concise oxidation process of heterostructured Ag@AuAg hollow NPs in a H2O2/PBS solution to generate AgCl nanocrystals and high-oxidation-state (hos) metal species. The hos/AgCl-assembled NPs offered a strong redox reaction to kill bacteria at 1.25 ppm[Ag] which was lower minimal inhibition concentration value than the utility of Ag ions and Ag NPs. A rapid meet-dip-kill process to disintegrate the bacterial membrane was observed within 60 min. The continuous release of Ag ions from AgCl blocks served as a smart bactericide to sustainably inhibit bacterial growth up to 7 days. The hos/AgCl-based bactericide induced enhanced evolution of a distinctive subpopulation with rigid membrane structure against both Ag ions and Ag-based NPs. This Ag-resistant persister behaved the downregulation of energy consumption and the physical insulation for Ag ions by secreting bio-reductants to convert Ag ions to less toxic Ag NPs. Based on our findings, hos/AgCl-assembled NPs endowed multiple antibacterial effects with no prominent findings of toxicity in the liver and kidneys, which opens a new era to understand the antimicrobial mechanism and resistant risk of Ag-related NPs for future clinical and environmental application.

AB - Although inorganic silver-based nanoparticles (NPs) have been used to replace antibiotics to treat environmental microorganisms, the silver ion diffusion mechanism takes at least hours to poison the bacteria and cannot destruct the bacteria immediately. In this paper, we developed a concise oxidation process of heterostructured Ag@AuAg hollow NPs in a H2O2/PBS solution to generate AgCl nanocrystals and high-oxidation-state (hos) metal species. The hos/AgCl-assembled NPs offered a strong redox reaction to kill bacteria at 1.25 ppm[Ag] which was lower minimal inhibition concentration value than the utility of Ag ions and Ag NPs. A rapid meet-dip-kill process to disintegrate the bacterial membrane was observed within 60 min. The continuous release of Ag ions from AgCl blocks served as a smart bactericide to sustainably inhibit bacterial growth up to 7 days. The hos/AgCl-based bactericide induced enhanced evolution of a distinctive subpopulation with rigid membrane structure against both Ag ions and Ag-based NPs. This Ag-resistant persister behaved the downregulation of energy consumption and the physical insulation for Ag ions by secreting bio-reductants to convert Ag ions to less toxic Ag NPs. Based on our findings, hos/AgCl-assembled NPs endowed multiple antibacterial effects with no prominent findings of toxicity in the liver and kidneys, which opens a new era to understand the antimicrobial mechanism and resistant risk of Ag-related NPs for future clinical and environmental application.

UR - http://www.scopus.com/inward/record.url?scp=85098657953&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85098657953&partnerID=8YFLogxK

U2 - 10.1016/j.cej.2020.128266

DO - 10.1016/j.cej.2020.128266

M3 - Article

AN - SCOPUS:85098657953

SN - 1385-8947

VL - 409

JO - Chemical Engineering Journal

JF - Chemical Engineering Journal

M1 - 128266

ER -

Multiplex antibacterial processes and risk in resistant phenotype by high oxidation-state nanoparticles: New killing process and mechanism investigations

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