Skip to main content
SpringerLink
Log in

Antibacterial Effect of Silver and Iron Oxide Nanoparticles in Combination with Antibiotics on E. coli K12

  • Published:
BioNanoScience Aims and scope Submit manuscript

Abstract

Antibiotic resistance is one of the main public health problems. The increase in the occurrence of multi-resistant pathogenic strains of bacteria due to biofilm formation gradually leads to inefficiency of traditional antibiotics. There are many strategies to combat biofilms, such as nanotechnologies. It is extremely important and relevant for nanomedicine to understand how the exposure of metal nanoparticles affects living organisms. The aim was to study the synergistic antibacterial activity of silver (AgNPs) and iron oxide (Fe3O4NPs) nanoparticles in combination with tetracycline (Tet) and ampicillin (Amp). The tests were performed against the wild strain E. coli K12. Our results suggest that both Fe3O4NPs and AgNPs form complexes with Amp and Tet. Fe3O4NPs slow down and AgNPs suppress the growth of E. coli at high concentrations. Dose-dependent inhibition of E. coli K12 growth is observed for AgNPs and Tet-AgNPs. The synergistic antibacterial effect is likely due to enhanced bacterial binding by AgNPs, which is assisted by Tet, but not by Amp. Fe3O4NPs do not exhibit bacterial growth inhibitory activity, but in combination with Amp, antagonism is observed. Fe3O4NPs slightly enhance the antibacterial effect of Tet. The antibacterial effect of Amp and Tet decreases when used in combination with AgNPs. Fe3O4NPs reduce the inhibitory effect of antibiotics on the formation of microcolonies. AgNPs suppress the growth of microcolonies, and in combination with Tet, the effects are enhanced. We hypothesize that the synergistic antibacterial activity correlates with the complex formation between NPs and the antibiotics. We propose pathways which lead to the synergistic effect.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  1. Ali, S. G., Ansari, M. A., Khan, H. M., Jalal, M., Mahdi, A. A., & Cameotra, S. (2017). Crataeva nurvala nanoparticles inhibit virulence factors and biofilm formation in clinical isolates of Pseudomonas aeruginosa. Journal of Basic Microbiology, 57(3), 193–203.

  2. Allahverdiyev, A., Kon, K., Abamor, E., Bagirova, M., & Rafailovich, M. (2011). Coping with antibiotic resistance: combining nanoparticles with antibiotics and other antimicrobial agents. Expert Review of Anti-Infective Therapy, 9(11), 1035–1052. https://doi.org/10.1586/eri.11.121.

    Article  Google Scholar 

  3. Ansari, M. A., Khan, H. M., Khan, A. A., Cameotra, S. S., & Alzohairy, M. A. (2015). Anti-biofilm efficacy of silver nanoparticles against MRSA and MRSE isolated from wounds in a tertiary care hospital. Indian Journal of Medical Microbiology, 33(1), 101–109. https://doi.org/10.4103/0255-0857.148402.

    Article  Google Scholar 

  4. Barapatre, A., Aadil, K., & Jha, H. (2016). Synergistic antibacterial and antibiofilm activity of silver nanoparticles biosynthesized by lignin-degrading fungus. Bioresour Bioprocess, 3, 8. https://doi.org/10.1186/s40643-016-0083-y.

    Article  Google Scholar 

  5. Bauer, A., Kirby, W., Sherris, J., & Turck, M. (1966). Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol, 45, 493–499.

    Article  Google Scholar 

  6. Borcherding, J., Baltrusaitis, J., Chen, H., Stebounova, L., Wu, C.-M., Rubasinghege, G., Mudunkotuwa, I., Caraballo, C., Zabner, J., Grassian, V., & Comellas, A. (2014). Iron oxide nanoparticles induce Pseudomonas aeruginosa growth, induce biofilm formation, and inhibit antimicrobial peptide function. Environmental Science Nano, 1, 123–132. https://doi.org/10.1039/C3EN00029J.

    Article  Google Scholar 

  7. Cerceo, E., Deitelzweig, S. B., Sherman, B. M., & Amin, A. N. (2016). Multidrug-resistant gram-negative bacterial infections in the hospital setting: overview, implications for clinical practice, and emerging treatment options. Microbial Drug Resistance, 22(5), 412–431. https://doi.org/10.1089/mdr.2015.0220.

    Article  Google Scholar 

  8. Chatterjee, S., Bandyopadhyay, A., & Sarkar, K. (2011). Effect of iron oxide and gold nanoparticles on bacterial growth leading towards biological application. Journal of Nanobiotechnology, 9, 34–41. https://doi.org/10.1186/1477-3155-9-34.

    Article  Google Scholar 

  9. Chopra, I., & Roberts, M. (2005). Tetracycline antibiotics: mode of action, applications, molecular biology and epidemiology of bacterial resistance. Microbiology and Molecular Biology Reviews, 65(2), 232–260.

    Article  Google Scholar 

  10. CLSI M100S. (2017). Performance standards for antimicrobial susceptibility testing, ed. In 27.

    Google Scholar 

  11. Davies, J., & Davies, D. (2010). Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews, 74(3), 417–433. https://doi.org/10.1128/MMBR.00016-10.

    Article  MathSciNet  Google Scholar 

  12. Deng, H., McShan, D., Zhang, Y., Sinha, S., Arslan, Z., Ray, P. C., & Yu, H. (2016). Mechanistic study of the synergistic antibacterial activity of combined silver nanoparticles and common antibiotics. Environmental Science & Technology, 50(16), 8840–8848. https://doi.org/10.1021/acs.est.6b00998.

    Article  Google Scholar 

  13. do Nascimento, T., de Jesus Oliveira, E., Basilio Junior, I., de Araujo -Junior, J., & Macedo, R. (2013). Short -term stability studies of ampicillin and cephalexin in aqueous solution and human plasma: application of least squares method in Arrhenius equation. Journal of Pharmaceutical and Biomedical Analysis, 73, 59–64. https://doi.org/10.1016/j.jpba.2012.04.010.

    Article  Google Scholar 

  14. Dorobantu, L., Fallone, C., Noble, A., Veinot, J., Ma, G., Goss, G., & Burrell, R. (2015). Toxicity of silver nanoparticles against bacteria, yeast, and algae. Journal of Nanoparticle Research, 17(4), 172–185. https://doi.org/10.1007/s11051-015-2984-7.

    Article  Google Scholar 

  15. Fazeli, H., Moghim, S., & Zare, D. (2018). Antimicrobial resistance pattern and spectrum of multiple-drug-resistant enterobacteriaceae in Iranian hospitalized patients with cancer. Advances in Biomedical Research, 7, 69. https://doi.org/10.4103/abr.abr_164_17.

    Article  Google Scholar 

  16. Fortunati, E., Latterini, L., Rinaldi, S., Kenny, J., & Armentano, I. (2011). PLGA/Ag nano-composites: in vitro degradation study and silver ion release. Journal of Materials Science. Materials in Medicine, 22(12), 2735–2744. https://doi.org/10.1007/s10856-011-4450-0.

    Article  Google Scholar 

  17. Ghosh, S., Patil, S., Ahire, M., Kitture, R., Kale, S., Pardesi, K., Cameotra, S., Bellare, J., Dhavale, D., & Jabgunde, A. (2012). Synthesis of silver nanoparticles using Dioscorea bulbifera tuber extract and evaluation of its synergistic potential in combination with antimicrobial agents. International Journal of Nanomedicine, 7, 483–496. https://doi.org/10.2147/IJN.S24793.

    Google Scholar 

  18. Gupta, D., Singh, A., & Khan, A. (2017). Nanoparticles as efflux pump and biofilm inhibitor to rejuvenate bactericidal effect of conventional antibiotics. Nanoscale Research Letters, 12, 454. https://doi.org/10.1186/s11671-017-2222-6.

    Article  Google Scholar 

  19. Hajipour, M., Fromm, K., Ashkarran, A., de Aberasturi, D., & de Larramendi, I. (2012). Antibacterial properties of nanoparticles. Trends in Biotechnology, 30(10), 499–511. https://doi.org/10.1016/j.tibtech.2012.06.004.

    Article  Google Scholar 

  20. Halawani, E. (2016). Nanomedicine opened new horizons for metal nanoparticles to treat multi-drug resistant organisms. International Journal of Current Microbiology and Applied Sciences, 5(2), 397–414.

    Article  Google Scholar 

  21. Hwang, I., Hwang, J., Choi, H., Kim, K., & Lee, D. (2012). Synergistic effects between silver nanoparticles and antibiotics and the mechanisms involved. Journal of Medical Microbiology, 61, 1719–1726. https://doi.org/10.1099/jmm.0.047100-0.

    Article  Google Scholar 

  22. Kalishwaralal, K., BarathManiKanth, S., Pandian, S. R., Deepak, V., & Gurunathan, S. (2010). Silver nanoparticles impede the biofilm formation by Pseudomonas aeruginosa and Staphylococcus epidermidis. Colloids and Surfaces. B, Biointerfaces, 79(2), 340–344. https://doi.org/10.1016/j.colsurfb.2010.04.014.

    Article  Google Scholar 

  23. Kang, F., Alvarez, P., & Zhu, D. (2014). Microbial extracellular polymeric substances reduce Ag+ to silver nanoparticles and antagonize bactericidal activity. Environmental Science & Technology, 48(1), 316–322. https://doi.org/10.1021/es403796x.

  24. Le Ouay, B., & Stellacci, F. (2015). Antibacterial activity of silver nanoparticles: a surface science insight. Nano Today, 10(3), 339–354. https://doi.org/10.1016/j.nantod.2015.04.002.

    Article  Google Scholar 

  25. Li, P., Li, J., Wu, C., Wu, Q., & Li, J. (2005). Synergistic effect of β-lactam antibiotic combined with silver nanoparticles. Nanotechnology, 16(9), 1912–1917. https://doi.org/10.1088/0957-4484/16/9/082.

  26. Liu, H., Zhao, Y., Zhao, D., Gong, T., Wu, Y., Han, H., Xu, T., Peschel, A., Han, S., & Qu, D. (2015). Antibacterial and anti-biofilm activities of thiazolidione derivatives against clinical staphylococcus strains. Emergency Microbes and Infection, 4(1), e1.

    Google Scholar 

  27. Lok, C.-N., Ho, C.-M., Chen, R., He, Q.-Y., Yu, W.-Y., Sun, H., Tam, P. K.-H., Chiu, J.-F., & Che, C.-M. (2006). Proteomic analysis of the mode of antibacterial action of silver nanoparticles. Journal of Proteome Research, 5(4), 916–924. https://doi.org/10.1021/pr0504079.

    Article  Google Scholar 

  28. Lu, W., Senapati, D., Wang, S., Tovmachenko, O., Singh, A., Yu, H., & Ray, P. (2010). Effect of surface coating on the toxicity of silver nanomaterials on human skin keratinocytes. Chemical Physics Letters, 487, 92–96. https://doi.org/10.1016/j.cplett.2010.01.027.

    Article  Google Scholar 

  29. Maillard, J. Y., & Hartemann, P. (2013). Silver as an antimicrobial: facts and gaps in knowledge. Critical Reviews in Microbiology, 39(4), 373–383. https://doi.org/10.3109/1040841X.2012.713323.

    Article  Google Scholar 

  30. McQuillan, J., Groenaga, I. H., Stokes, E., & Shaw, A. (2012). Silver nanoparticle enhanced silver ion stress response in Escherichia coli K12. Nanotoxicology, 6(8), 857–866. https://doi.org/10.3109/17435390.2011.626532.

    Article  Google Scholar 

  31. McShana, D., Zhanga, Y., Denga, H., Raya, P., & Yua, H. (2015). Synergistic antibacterial effect of silver nanoparticles combined with ineffective antibiotics on drug resistant Salmonella typhimurium DT104. Journal of Environmental Science and Health. Part C, Environmental Carcinogenesis & Ecotoxicology Reviews, 33(3), 369–384. https://doi.org/10.1080/10590501.2015.1055165.

    Article  Google Scholar 

  32. Morones, J., Elechiguerra, J., Camacho, A., & Ramirez, J. (2005). The bactericidal effect of silver nanoparticles. Nanotechnology, 16(10), 2346–2353. https://doi.org/10.1088/0957-4484/16/10/059.

    Article  Google Scholar 

  33. Mouton, J., & Vinks, A. (2007). Continuous infusion of beta – lactams. Current Opinion in Critical Care, 13(5), 598–606. https://doi.org/10.1097/MCC.0b013e3282e2a98f.

    Article  Google Scholar 

  34. Radzig, M., Nadtochenko, V., Koksharova, O., Kiwi, J., Lipasova, V., & Khmel, I. (2013). Antibacterial effects of silver nanoparticles on gram-negative bacteria: influence on the growth and biofilms formation, mechanisms of action. Colloids and Surfaces, B: Biointerfaces, 102, 300–306. https://doi.org/10.1016/j.colsurfb.2012.07.039.

    Article  Google Scholar 

  35. Rai, M., Yadav, A., & Gade, A. (2009). Silver nanoparticles as a new generation of antimicrobials. Biotechnology Advances, 27(1), 76–83. https://doi.org/10.1016/j.biotechadv.2008.09.002.

    Article  Google Scholar 

  36. Shete, P., Patil, R., Tiwale, B., & Pawar, S. (2015). Water dispersible oleic acid-coated Fe3O4 nanoparticles for biomedical applications. Journal of Magnetism and Magnetic Materials, 377, 406–410. https://doi.org/10.1016/j.jmmm.2014.10.137.

    Article  Google Scholar 

  37. Sondi, I., & Salopek-Sondi, B. (2004). Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. Journal of Colloid and Interface Science, 275(1), 177–182. https://doi.org/10.1016/j.jcis.2004.02.012.

    Article  Google Scholar 

  38. Vardanyan, Z., Gevorkyan, V., Ananyan, M., Vardapetyan, H., & Trchounian, A. (2015). Effects of various heavy metal nanoparticles on Enterococcus hirae and Escherichia coli growth and proton-coupled membrane transport. Journal of Nanbiotechnology, 13, 69. https://doi.org/10.1186/s12951-015-0131-3.

    Article  Google Scholar 

  39. Xiu, Z., Ma, J., & Alvarez, P. (2011). Differential effect of common ligands and molecular oxygen on antimicrobial activity of silver nanoparticles versus silver ions. Environmental Science & Technology, 45(20), 9003–9008. https://doi.org/10.1021/es201918f.

    Article  Google Scholar 

  40. Xu, H., Qu, F., Xu, H., Lai, W., Wang, Y., Aguilar, Z., & Wei, H. (2012). Role of reactive oxygen species in the antibacterial mechanism of silver nanoparticles on Escherichia coli O157:H7. BioMetals., 25(1), 45–53. https://doi.org/10.1007/s10534-011-9482-x.

    Article  Google Scholar 

  41. Zhao, C., & Wang, W. (2012). Importance of surface coatings and soluble silver in silver nanoparticles toxicity to Daphnia magna. Nanotoxicology, 6(4), 361–370. https://doi.org/10.3109/17435390.2011.579632.

    Article  Google Scholar 

  42. Zhuang, L., Zhang, W., Zhao, Y., Shen, H., Lin, H., & Liang, J. (2015). Preparation and characterization of Fe3O4 particles with novel nanosheets morphology and magnetochromatic property by a modified solvothermal method. Scientific Reports, 5, 9320. https://doi.org/10.1038/srep09320.

Download references

Acknowledgements

The authors thank Rshtuni L (Russian-Armenian University) for the help with synthesis of nanoparticles. The work was performed in the framework of the Program for Basic Research of Russian State Academies of Sciences for 2018.

Author information

Authors and Affiliations

  1. Laboratory of Analytical biochemistry and Biotechnology, Department of Medical Biochemistry and Biotechnology, Russian-Armenian University, H. Emin 123, Yerevan, Republic of Armenia

    Khachatryan Anush, Kazaryan Shushanik, Tiratsuyan Susanna & Hovhannisyan Ashkhen

Authors
  1. Khachatryan Anush
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kazaryan Shushanik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tiratsuyan Susanna
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hovhannisyan Ashkhen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hovhannisyan Ashkhen.

Ethics declarations

Conflict of Interest

None.

Research Involving Humans and Animals Statement

None.

Informed Consent

None.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Anush, K., Shushanik, K., Susanna, T. et al. Antibacterial Effect of Silver and Iron Oxide Nanoparticles in Combination with Antibiotics on E. coli K12. BioNanoSci. 9, 587–596 (2019). https://doi.org/10.1007/s12668-019-00640-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12668-019-00640-0

Keywords

Search

Navigation