Antibacterial Action of Zn2+ Ions Driven by the In Vivo Formed ZnO Nanoparticles

Toni Vitasovic; Giada Caniglia; Neda Eghtesadi; Marcel Ceccato; Espen Drath Bo̷jesen; Ulrich Gosewinkel; Gregor Neusser; Ulrich Rupp; Paul Walther; Christine Kranz; Elena E. Ferapontova

doi:10.1021/acsami.4c04682

Antibacterial Action of Zn²⁺ Ions Driven by the In Vivo Formed ZnO Nanoparticles

Toni Vitasovic, Giada Caniglia, Neda Eghtesadi, Marcel Ceccato, Espen Drath Bo̷jesen, Ulrich Gosewinkel, Gregor Neusser, Ulrich Rupp, Paul Walther, Christine Kranz, Elena E. Ferapontova^*

^*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

21 Citationer (Scopus)

Abstract

Antibacterial formulations based on zinc oxide nanoparticles (ZnO NPs) are widely used for antibiotic replacement in veterinary medicine and animal nutrition. However, the undesired environmental impact of ZnO NPs triggers a search for alternative, environmentally safer solutions. Here, we show that Zn²⁺ in its ionic form is a more eco-friendly antibacterial, and its biocidal action rivals that of ZnO NPs (<100 nm size), with a minimal biocidal concentration being 41(82) μg mL^-1 vs 5 μg mL^-1 of ZnO NPs, as determined for 10³(10⁶) CFU mL^-1 E. coli. We demonstrate that the biocidal activity of Zn²⁺ ions is primarily associated with their uptake by E. coli and spontaneous in vivo transformation into insoluble ZnO nanocomposites at an internal bacterial pH of 7.7. Formed in vivo nanocomposite then damages E. coli membrane and intracellular components from the inside, by forming insoluble biocomposites, whose formation can also trigger ZnO characteristic reactions damaging the cells (e.g., by generation of high-potential reactive oxygen species). Our study defines a special route in which Zn²⁺ metal ions induce the death of bacterial cells, which might be common to other metal ions capable of forming semiconductor oxides and insoluble hydroxides at a slightly alkaline intracellular pH of some bacteria.

Originalsprog	Engelsk
Tidsskrift	ACS Applied Materials and Interfaces
Vol/bind	16
Nummer	24
Sider (fra-til)	30847-30859
Antal sider	13
ISSN	1944-8244
DOI	https://doi.org/10.1021/acsami.4c04682
Status	Udgivet - jun. 2024

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10.1021/acsami.4c04682

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Citationsformater

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title = "Antibacterial Action of Zn2+ Ions Driven by the In Vivo Formed ZnO Nanoparticles",

abstract = "Antibacterial formulations based on zinc oxide nanoparticles (ZnO NPs) are widely used for antibiotic replacement in veterinary medicine and animal nutrition. However, the undesired environmental impact of ZnO NPs triggers a search for alternative, environmentally safer solutions. Here, we show that Zn2+ in its ionic form is a more eco-friendly antibacterial, and its biocidal action rivals that of ZnO NPs (<100 nm size), with a minimal biocidal concentration being 41(82) μg mL-1 vs 5 μg mL-1 of ZnO NPs, as determined for 103(106) CFU mL-1 E. coli. We demonstrate that the biocidal activity of Zn2+ ions is primarily associated with their uptake by E. coli and spontaneous in vivo transformation into insoluble ZnO nanocomposites at an internal bacterial pH of 7.7. Formed in vivo nanocomposite then damages E. coli membrane and intracellular components from the inside, by forming insoluble biocomposites, whose formation can also trigger ZnO characteristic reactions damaging the cells (e.g., by generation of high-potential reactive oxygen species). Our study defines a special route in which Zn2+ metal ions induce the death of bacterial cells, which might be common to other metal ions capable of forming semiconductor oxides and insoluble hydroxides at a slightly alkaline intracellular pH of some bacteria.",

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author = "Toni Vitasovic and Giada Caniglia and Neda Eghtesadi and Marcel Ceccato and Bo̷jesen, {Espen Drath} and Ulrich Gosewinkel and Gregor Neusser and Ulrich Rupp and Paul Walther and Christine Kranz and Ferapontova, {Elena E.}",

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T1 - Antibacterial Action of Zn2+ Ions Driven by the In Vivo Formed ZnO Nanoparticles

AU - Vitasovic, Toni

AU - Caniglia, Giada

AU - Eghtesadi, Neda

AU - Ceccato, Marcel

AU - Bo̷jesen, Espen Drath

AU - Gosewinkel, Ulrich

AU - Neusser, Gregor

AU - Rupp, Ulrich

AU - Walther, Paul

AU - Kranz, Christine

AU - Ferapontova, Elena E.

PY - 2024/6

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N2 - Antibacterial formulations based on zinc oxide nanoparticles (ZnO NPs) are widely used for antibiotic replacement in veterinary medicine and animal nutrition. However, the undesired environmental impact of ZnO NPs triggers a search for alternative, environmentally safer solutions. Here, we show that Zn2+ in its ionic form is a more eco-friendly antibacterial, and its biocidal action rivals that of ZnO NPs (<100 nm size), with a minimal biocidal concentration being 41(82) μg mL-1 vs 5 μg mL-1 of ZnO NPs, as determined for 103(106) CFU mL-1 E. coli. We demonstrate that the biocidal activity of Zn2+ ions is primarily associated with their uptake by E. coli and spontaneous in vivo transformation into insoluble ZnO nanocomposites at an internal bacterial pH of 7.7. Formed in vivo nanocomposite then damages E. coli membrane and intracellular components from the inside, by forming insoluble biocomposites, whose formation can also trigger ZnO characteristic reactions damaging the cells (e.g., by generation of high-potential reactive oxygen species). Our study defines a special route in which Zn2+ metal ions induce the death of bacterial cells, which might be common to other metal ions capable of forming semiconductor oxides and insoluble hydroxides at a slightly alkaline intracellular pH of some bacteria.

AB - Antibacterial formulations based on zinc oxide nanoparticles (ZnO NPs) are widely used for antibiotic replacement in veterinary medicine and animal nutrition. However, the undesired environmental impact of ZnO NPs triggers a search for alternative, environmentally safer solutions. Here, we show that Zn2+ in its ionic form is a more eco-friendly antibacterial, and its biocidal action rivals that of ZnO NPs (<100 nm size), with a minimal biocidal concentration being 41(82) μg mL-1 vs 5 μg mL-1 of ZnO NPs, as determined for 103(106) CFU mL-1 E. coli. We demonstrate that the biocidal activity of Zn2+ ions is primarily associated with their uptake by E. coli and spontaneous in vivo transformation into insoluble ZnO nanocomposites at an internal bacterial pH of 7.7. Formed in vivo nanocomposite then damages E. coli membrane and intracellular components from the inside, by forming insoluble biocomposites, whose formation can also trigger ZnO characteristic reactions damaging the cells (e.g., by generation of high-potential reactive oxygen species). Our study defines a special route in which Zn2+ metal ions induce the death of bacterial cells, which might be common to other metal ions capable of forming semiconductor oxides and insoluble hydroxides at a slightly alkaline intracellular pH of some bacteria.

KW - antibacterial activity

KW - E. coli

KW - environmental safety

KW - nanotoxicity

KW - Zn ions

KW - ZnO nanoparticles

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