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Particle-cell contact enhances antibacterial activity of silver nanoparticles.
PLoS One. 2013; 8(5):e64060.Plos

Abstract

BACKGROUND

It is generally accepted that antibacterial properties of Ag nanoparticles (AgNPs) are dictated by their dissolved fraction. However, dissolution-based concept alone does not fully explain the toxic potency of nanoparticulate silver compared to silver ions.

METHODOLOGY/PRINCIPAL FINDINGS

Herein, we demonstrated that the direct contact between bacterial cell and AgNPs' surface enhanced the toxicity of nanosilver. More specifically, cell-NP contact increased the cellular uptake of particle-associated Ag ions - the single and ultimate cause of toxicity. To prove that, we evaluated the toxicity of three different AgNPs (uncoated, PVP-coated and protein-coated) to six bacterial strains: Gram-negative Escherichia coli, Pseudomonas fluorescens, P. putida and P. aeruginosa and Gram-positive Bacillus subtilis and Staphylococcus aureus. While the toxicity of AgNO3 to these bacteria varied only slightly (the 4-h EC50 ranged from 0.3 to 1.2 mg Ag/l), the 4-h EC50 values of protein-coated AgNPs for various bacterial strains differed remarkably, from 0.35 to 46 mg Ag/l. By systematically comparing the intracellular and extracellular free Ag(+) liberated from AgNPs, we demonstrated that not only extracellular dissolution in the bacterial test environment but also additional dissolution taking place at the particle-cell interface played an essential role in antibacterial action of AgNPs. The role of the NP-cell contact in dictating the antibacterial activity of Ag-NPs was additionally proven by the following observations: (i) separation of bacterial cells from AgNPs by particle-impermeable membrane (cut-off 20 kDa, ∼4 nm) significantly reduced the toxicity of AgNPs and (ii) P. aeruginosa cells which tended to attach onto AgNPs, exhibited the highest sensitivity to all forms of nanoparticulate Ag.

CONCLUSIONS/SIGNIFICANCE

Our findings provide new insights into the mode of antibacterial action of nanosilver and explain some discrepancies in this field, showing that "Ag-ion" and "particle-specific" mechanisms are not controversial but, rather, are two faces of the same coin.

Authors+Show Affiliations

Laboratory of Environmental Toxicology, National Institute of Chemical Physics and Biophysics, Tallinn, Estonia. olesja.bondarenko@kbfi.eeNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

23737965

Citation

Bondarenko, Olesja, et al. "Particle-cell Contact Enhances Antibacterial Activity of Silver Nanoparticles." PloS One, vol. 8, no. 5, 2013, pp. e64060.
Bondarenko O, Ivask A, Käkinen A, et al. Particle-cell contact enhances antibacterial activity of silver nanoparticles. PLoS One. 2013;8(5):e64060.
Bondarenko, O., Ivask, A., Käkinen, A., Kurvet, I., & Kahru, A. (2013). Particle-cell contact enhances antibacterial activity of silver nanoparticles. PloS One, 8(5), e64060. https://doi.org/10.1371/journal.pone.0064060
Bondarenko O, et al. Particle-cell Contact Enhances Antibacterial Activity of Silver Nanoparticles. PLoS One. 2013;8(5):e64060. PubMed PMID: 23737965.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Particle-cell contact enhances antibacterial activity of silver nanoparticles. AU - Bondarenko,Olesja, AU - Ivask,Angela, AU - Käkinen,Aleksandr, AU - Kurvet,Imbi, AU - Kahru,Anne, Y1 - 2013/05/30/ PY - 2013/01/14/received PY - 2013/04/08/accepted PY - 2013/6/6/entrez PY - 2013/6/6/pubmed PY - 2014/1/11/medline SP - e64060 EP - e64060 JF - PloS one JO - PLoS One VL - 8 IS - 5 N2 - BACKGROUND: It is generally accepted that antibacterial properties of Ag nanoparticles (AgNPs) are dictated by their dissolved fraction. However, dissolution-based concept alone does not fully explain the toxic potency of nanoparticulate silver compared to silver ions. METHODOLOGY/PRINCIPAL FINDINGS: Herein, we demonstrated that the direct contact between bacterial cell and AgNPs' surface enhanced the toxicity of nanosilver. More specifically, cell-NP contact increased the cellular uptake of particle-associated Ag ions - the single and ultimate cause of toxicity. To prove that, we evaluated the toxicity of three different AgNPs (uncoated, PVP-coated and protein-coated) to six bacterial strains: Gram-negative Escherichia coli, Pseudomonas fluorescens, P. putida and P. aeruginosa and Gram-positive Bacillus subtilis and Staphylococcus aureus. While the toxicity of AgNO3 to these bacteria varied only slightly (the 4-h EC50 ranged from 0.3 to 1.2 mg Ag/l), the 4-h EC50 values of protein-coated AgNPs for various bacterial strains differed remarkably, from 0.35 to 46 mg Ag/l. By systematically comparing the intracellular and extracellular free Ag(+) liberated from AgNPs, we demonstrated that not only extracellular dissolution in the bacterial test environment but also additional dissolution taking place at the particle-cell interface played an essential role in antibacterial action of AgNPs. The role of the NP-cell contact in dictating the antibacterial activity of Ag-NPs was additionally proven by the following observations: (i) separation of bacterial cells from AgNPs by particle-impermeable membrane (cut-off 20 kDa, ∼4 nm) significantly reduced the toxicity of AgNPs and (ii) P. aeruginosa cells which tended to attach onto AgNPs, exhibited the highest sensitivity to all forms of nanoparticulate Ag. CONCLUSIONS/SIGNIFICANCE: Our findings provide new insights into the mode of antibacterial action of nanosilver and explain some discrepancies in this field, showing that "Ag-ion" and "particle-specific" mechanisms are not controversial but, rather, are two faces of the same coin. SN - 1932-6203 UR - https://www.unboundmedicine.com/medline/citation/23737965/Particle_cell_contact_enhances_antibacterial_activity_of_silver_nanoparticles_ L2 - https://dx.plos.org/10.1371/journal.pone.0064060 DB - PRIME DP - Unbound Medicine ER -