Applied Microbiology and Biotechnology

, Volume 91, Issue 1, pp 153–162 | Cite as

The antibacterial activity of biogenic silver and its mode of action

  • Liesje Sintubin
  • Bart De Gusseme
  • Paul Van der Meeren
  • Benny F. G. Pycke
  • Willy Verstraete
  • Nico Boon
Applied Microbial and Cell Physiology

Abstract

In a previous study, biogenic silver nanoparticles were produced by Lactobacillus fermentum which served as a matrix preventing aggregation. In this study the antibacterial activity of this biogenic silver was compared to ionic silver and chemically produced nanosilver. The minimal inhibitory concentration (MIC) was tested on Gram-positive and Gram-negative bacteria and was comparable for biogenic silver and ionic silver ranging from 12.5 to 50 mg/L. In contrast, chemically produced nanosilver had a much higher MIC of at least 500 mg/L, due to aggregation upon application. The minimal bactericidal concentration (MBC) in drinking water varied from 0.1 to 0.5 mg/L for biogenic silver and ionic silver, but for chemically produced nanosilver concentrations, up to 12.5 mg/L was needed. The presence of salts and organic matter decreased the antimicrobial activity of all types of silver resulting in a higher MBC and a slower inactivation of the bacteria. The mode of action of biogenic silver was mainly attributed to the release of silver ions due to the high concentration of free silver ions measured and the resemblance in performance between biogenic silver and ionic silver. Radical formation by biogenic silver and direct contact were found to contribute little to the antibacterial activity. In conclusion, biogenic nanosilver exhibited equal antimicrobial activity compared to ionic silver and can be a valuable alternative for chemically produced nanosilver.

Keywords

Biocide Nanoparticles Green chemistry Biological synthesis Drinking water Disinfectant 

Supplementary material

253_2011_3225_MOESM1_ESM.doc (216 kb)
Fig. S1Setups to test direct contact as one of the possible modes of action. a Setup 1 where biogenic silver was added in a dialysis membrane preventing direct contact with E. coli in the surrounding drinking water. b Setup 2 where biogenic silver and E. coli were added together to the Erlemeyer and therefore direct contact was possible; an empty dialysis membrane was present to account for possible sorption of silver ions. Biogenic silver is presented by dashed lines (DOC 216 kb)
253_2011_3225_MOESM2_ESM.doc (412 kb)
Fig. S2Scanning electron microscopy image of biogenic silver. The black dots are silver nanoparticles attached on the cell wall of the bacterial carrier L. fermentum. The bacterium looks black due to closely packed layers of silver nanoparticles covering its surface (DOC 412 kb)

References

  1. Bagg J (1962) The catalytic decomposition of hydrogen peroxide solutions by single crystals of silver. Aust J Chem 15:201–210CrossRefGoogle Scholar
  2. Benn TM, Westerhoff P (2008) Nanoparticle silver released into water from commercially available sock fabrics. Environ Sci Technol 42:4133–4139CrossRefGoogle Scholar
  3. Boon N, Depuydt S, Verstraete W (2006) Evolutionary algorithms and flow cytometry to examine the parameters influencing transconjugant formation. FEMS Microbiol Ecol 55:17–27CrossRefGoogle Scholar
  4. Boorman GA, Dellarco V, Dunnick JK, Chapin RE, Hunter S, Hauchman F, Gardner H, Cox M, Sills RC (1999) Drinking water disinfection byproducts: review and approach to toxicity evaluation. Environ Health Perspect 107:207–217Google Scholar
  5. Choi O, Hu Z (2009) Role of reactive oxygen species in determining nitrification inhibition by metallic/oxide nanoparticles. J Environ Eng 135:1365–1370CrossRefGoogle Scholar
  6. De Gusseme B, Sintubin L, Baert L, Thibo E, Hennebel T, Vermeulen G, Uyttendaele M, Verstraete W, Boon N (2010) Biogenic silver for disinfection of water contaminated with viruses. Appl Environ Microbiol 76:1082–1087CrossRefGoogle Scholar
  7. Edwards-Jones V (2009) The benefits of silver in hygiene, personal care and healthcare. Lett Appl Microbiol 49:147–152CrossRefGoogle Scholar
  8. Elechiguerra JL, Burt JL, Morones JR, Camacho-Bragado A, Gao X, Lara HH, Yacaman MJ (2005) Interaction of silver nanoparticles with HIV-1. J Nanobiotechnol 3:6CrossRefGoogle Scholar
  9. Feng QL, Wu J, Chen GQ, Cui FZ, Kim TN, Kim JO (2000) A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J Biomed Mater Res 52:662–668CrossRefGoogle Scholar
  10. Fu MX, Li QB, Sun DH, Lu YH, He N, Deng X, Wang HX, Huang JL (2006) Rapid preparation process of silver nanoparticles by bioreduction and their characterizations. Chin J Chem Eng 14:114–117CrossRefGoogle Scholar
  11. Gerber IB, Dubery IA (2003) Fluorescence microplate assay for the detection of oxidative burst products in tobacco cell suspensions using 2′,7′-dichlorofluorescein. Methods Cell Sci 25:115–122CrossRefGoogle Scholar
  12. Gopal K, Tripathy SS, Bersillon JL, Dubey SP (2007) Chlorination byproducts, their toxicodynamics and removal from drinking water. J Hazard Mater 140:1–6CrossRefGoogle Scholar
  13. Hennebel T, De Gusseme B, Boon N, Verstraete W (2009) Biogenic metals in advanced water treatment. Trends Biotechnol 27:90–98CrossRefGoogle Scholar
  14. Holt KB, Bard AJ (2005) Interaction of silver(I) ions with the respiratory chain of Escherichia coli: an electrochemical and scanning electrochemical microscopy study of the antimicrobial mechanism of micromolar Ag. Biochemistry 44:13214–13223CrossRefGoogle Scholar
  15. Kathiresan K, Manivannan S, Nabeel MA, Dhivya B (2009) Studies on silver nanoparticles synthesized by a marine fungus, Penicillium fellutanum isolated from coastal mangrove sediment. Colloid Surf B Biointerfaces 71:133–137CrossRefGoogle Scholar
  16. Kim JS, Kuk E, Yu KN, Kim JH, Park SJ, Lee HJ, Kim SH, Park YK, Park YH, Hwang CY, Kim YK, Lee YS, Jeong DH, Cho MH (2007) Antimicrobial effects of silver nanoparticles. Nanomed Nanotechnol Biol Med 3:95–101CrossRefGoogle Scholar
  17. Klaus T, Joerger R, Olsson E, Granqvist CG (1999) Silver-based crystalline nanoparticles, microbially fabricated. Proc Natl Acad Sci USA 96:13611–13614CrossRefGoogle Scholar
  18. Kumar SA, Abyaneh MK, Gosavi SW, Kulkarni SK, Pasricha R, Ahmad A, Khan MI (2007) Nitrate reductase-mediated synthesis of silver nanoparticles from AgNO3. Biotechnol Lett 29:439–445CrossRefGoogle Scholar
  19. Kwakye-Awuah B, Williams C, Kenward MA, Radecka I (2008) Antimicrobial action and efficiency of silver-loaded zeolite X. J Appl Microbiol 104:1516–1524CrossRefGoogle Scholar
  20. Lansdown ABG (2007) Critical observations on the neurotoxicity of silver. Crit Rev Toxicol 37:237–250CrossRefGoogle Scholar
  21. Li QL, Mahendra S, Lyon DY, Brunet L, Liga MV, Li D, Alvarez PJJ (2008) Antimicrobial nanomaterials for water disinfection and microbial control: potential applications and implications. Water Res 42:4591–4602CrossRefGoogle Scholar
  22. Liau SY, Read DC, Pugh WJ, Furr JR, Russell AD (1997) Interaction of silver nitrate with readily identifiable groups: relationship to the antibacterial action of silver ions. Lett Appl Microbiol 25:279–283CrossRefGoogle Scholar
  23. Liu J, Hurt RH (2010) Ion release kinetics and particle persistence in aqueous nano-silver colloids. Environ Sci Technol 44:2169–2175CrossRefGoogle Scholar
  24. Lok CN, Ho CM, Chen R, He QY, Yu WY, Sun H, Tam PKH, Chiu JF, Che CM (2007) Silver nanoparticles: partial oxidation and antibacterial activities. J Biol Inorg Chem 12:527–534CrossRefGoogle Scholar
  25. Mafune F, J-y K, Takeda Y, Kondow T, Sawabe H (2000) Structure and stability of silver nanoparticles in aqueous solution produced by laser ablation. J Phys Chem B 104:8333–8337CrossRefGoogle Scholar
  26. Matsumura Y, Yoshikata K, Kunisaki S, Tsuchido T (2003) Mode of bactericidal action of silver zeolite and its comparison with that of silver nitrate. Appl Environ Microbiol 69:4278–4281CrossRefGoogle Scholar
  27. Maynard AD (2007) Nanotechnologies: overview and issues. In: Simeonova PP, Opopol N, Luster MI (eds) Nanotechnology—toxicological issues and environmental safety. Nato science for peace and security series C: environmental security. Springer, Dordrecht, pp 1–14Google Scholar
  28. Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramirez JT, Yacaman MJ (2005) The bactericidal effect of silver nanoparticles. Nanotechnology 16:2346–2353CrossRefGoogle Scholar
  29. Mukherjee P, Ahmad A, Mandal D, Senapati S, Sainkar SR, Khan MI, Parishcha R, Ajaykumar PV, Alam M, Kumar R, Sastry M (2001) Fungus-mediated synthesis of silver nanoparticles and their immobilization in the mycelial matrix: a novel biological approach to nanoparticle synthesis. Nano Lett 1:515–519CrossRefGoogle Scholar
  30. Nanavaty J, Mortensen JE, Shryock TR (1998) The effects of environmental conditions on the in vitro activity of selected antimicrobial agents against Escherichia coli. Curr Microbiol 36:212–215CrossRefGoogle Scholar
  31. NEN-EN (1997) Chemical disinfectants and antiseptics—quantitative suspension test for the evaluation of bactericidal activity of chemical disinfectants and antiseptics used in food, industrial, domestic, and institutional areas—test method and requirements (phase 2, step1), vol 1276. European committee for standardization, BrusselsGoogle Scholar
  32. Pal S, Tak YK, Song JM (2007) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli. Appl Environ Microbiol 73:1712–1720CrossRefGoogle Scholar
  33. Shahverdi AR, Minaeian S, Shahverdi HR, Jamalifar H, Nohi AA (2007) Rapid synthesis of silver nanoparticles using culture supernatants of Enterobacteria: a novel biological approach. Process Biochem 42:919–923CrossRefGoogle Scholar
  34. Silver S, le Phung T, Silver G (2006) Silver as biocides in burn and wound dressings and bacterial resistance to silver compounds. J Ind Microbiol Biotechnol 33:627–634CrossRefGoogle Scholar
  35. Sintubin L, De Windt W, Dick J, Mast J, van der Ha D, Verstraete W, Boon N (2009) Lactic acid bacteria as reducing and capping agent for the fast and efficient production of silver nanoparticles. Appl Microbiol Biotechnol 84:741–749CrossRefGoogle Scholar
  36. Sondi I, Salopek-Sondi B (2004) Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J Colloid Interface Sci 275:177–182CrossRefGoogle Scholar
  37. Sotiriou GA, Pratsinis SE (2010) Antibacterial activity of nanosilver ions and particles. Environ Sci Technol 44:5649–5654CrossRefGoogle Scholar
  38. Su H-L, Chou C-C, Hung D-J, Lin S-H, Pao IC, Lin J-H, Huang F-L, Dong R-X, Lin J-J (2009) The disruption of bacterial membrane integrity through ROS generation induced by nanohybrids of silver and clay. Biomaterials 30:5979–5987CrossRefGoogle Scholar
  39. Tavakoli A, Sohrabi M, Kargari A (2007) A review of methods for synthesis of nanostructured metals with emphasis on iron compounds. Chem Paper 61:151–170CrossRefGoogle Scholar
  40. Yoon KY, Byeon JH, Park JH, Hwang J (2007) Susceptibility constants of Escherichia coli and Bacillus subtilis to silver and copper nanoparticles. Sci Total Environ 373:572–575CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Liesje Sintubin
    • 1
  • Bart De Gusseme
    • 1
  • Paul Van der Meeren
    • 2
  • Benny F. G. Pycke
    • 1
  • Willy Verstraete
    • 1
  • Nico Boon
    • 1
  1. 1.Laboratory of Microbial Ecology and Technology (LabMET)Ghent UniversityGentBelgium
  2. 2.Particle and Interfacial Technology GroupGhent UniversityGentBelgium

Personalised recommendations