Selective Antimicrobial Performance of Biosynthesized Silver Nanoparticles by Horsetail Extract Against E. coli

  • Miona Miljković
  • Vesna LazićEmail author
  • Slađana Davidović
  • Ana Milivojević
  • Jelena Papan
  • Margarida M. Fernandes
  • Senentxu Lanceros-Mendez
  • S. Phillip Ahrenkiel
  • Jovan M. Nedeljković


The aim of this study was the development of a non-toxic, biosynthetic antimicrobial agent which selectively acts on only one type of microorganism, and preserves the microbiota. Antimicrobial performance of biosynthesized silver nanoparticles (Ag NPs) by horsetail (Equisetum arvense L.) extract was examined against Gram-negative bacteria Escherichia coli and Gram-positive bacteria Staphylococcus aureus, as well as yeasts Candida albicans and Saccharomyces boulardii. Also, the cytotoxicity of Ag NPs was examined toward pre-osteoblast cells. The synthetic conditions—concentration of extract, temperature, and pH—were optimized to prepare silver colloids with different particle size distributions and long-term stability. The obtained samples were characterized using transmission electron microscopy, X-ray diffraction analysis, and absorption spectroscopy. The smaller-sized Ag NPs (~ 10–20 nm), prepared at a lower temperature (20 °C), showed better antimicrobial performance against E. coli compared to larger ones (~ 40–60 nm), prepared at high temperature (100 °C). On the other hand, both samples did not display any toxic action against bacteria S. aureus, or yeasts C. albicans and S. boulardii. Non-cytotoxic behavior of Ag NPs toward pre-osteoblast cells was observed for the concentrations of silver ≤ 2.25 and ≤ 4.5 mg L−1 for 10–20 and 40–60 nm-sized Ag NPs, respectively. Biosynthesized Ag NPs by horsetail extract display selective toxic action against E. coli at the ecologically acceptable concentration level.


Silver nanoparticles Horsetail extract Antimicrobial activity Green synthesis Cytotoxicity 



Financial support for this study was granted by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Projects III 45020 and TR 31035).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Supplementary material 1 (DOCX 1152 kb)


  1. 1.
    C.J. Murphy, T.K. Sau, A.M. Gole, C.J. Orendorff, J. Gao, L. Gou, S.E. Hunyadi, T. Li, Anisotropic metal nanoparticles: synthesis, assembly, and optical applications. J. Phys. Chem. B 109, 13857–13870 (2005)PubMedCrossRefGoogle Scholar
  2. 2.
    A. Panaček, L. Kvitek, R. Prucek, M. Kolar, R. Večerova, N. Pizurova, V.K. Sharma, T. Nevečna, R. Zboril, Silver colloid nanoparticles: synthesis, characterization, and their antibacterial activity. J. Phys. Chem. B 110, 16248–16253 (2006)PubMedCrossRefGoogle Scholar
  3. 3.
    S. Pal, Y.K. Tak, J.M. Song, 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. Microb. 73, 1712–1720 (2007)CrossRefGoogle Scholar
  4. 4.
    M. Rai, A. Yadav, A. Gade, Silver nanoparticles as a new generation of antimicrobials. Biotechnol. Adv. 27, 76–83 (2009)PubMedCrossRefGoogle Scholar
  5. 5.
    V. Ilić, Z.V. Šaponjić, V.V. Vodnik, B. Potkonjak, P. Jovančić, J.M. Nedeljković, M. Radetić, The influence of silver content on antimicrobial activity and color of cotton fabrics functionalized with Ag nanoparticles. Carbohyd. Polym. 78, 564–569 (2009)CrossRefGoogle Scholar
  6. 6.
    M. Radetić, V. Ilić, V.V. Vodnik, S. Dimitrijević, P. Jovančić, Z.V. Šaponjić, J.M. Nedeljković, Antibacterial effect of silver nanoparticles deposited on corona-treated polyester and polyamide fabrics. Polym. Adv. Technol. 19, 1816–1821 (2008)CrossRefGoogle Scholar
  7. 7.
    V. Ilić, Z. Šaponjić, V. Vodnik, D. Mihailović, P. Jovančić, M. Radetić, A study of the antibacterial efficiency and coloration of dyed polyamide and polyester fabrics modified with colloidal Ag nanoparticles. J. Serb. Chem. Soc. 74, 349–357 (2009)CrossRefGoogle Scholar
  8. 8.
    Y.-M. Cho, Y. Mizuta, J.-I. Akagi, T. Toyoda, M. Sone, K. Ogawa, Size-dependent acute toxicity of silver nanoparticles in mice. J. Toxicol. Pathol. 31, 73–80 (2018)PubMedCrossRefGoogle Scholar
  9. 9.
    R. Vazquez-Muñoz, B. Borrego, K. Juárez-Moreno, M. García-García, J.D. Mota Morales, N. Bogdanchikova, A. Huerta-Saquero, Toxicity of silver nanoparticles in biological systems: does the complexity of biological systems matter? Toxicol. Lett. 276, 11–20 (2017)PubMedCrossRefGoogle Scholar
  10. 10.
    V.V. Vukovic, J.M. Nedeljkovic, Surface modification of nanometer-scale silver particles by imidazole. Langmuir 9, 980–983 (1993)CrossRefGoogle Scholar
  11. 11.
    S. Onitsuka, T. Hamada, H. Okamura, Preparation of antimicrobial gold and silver nanoparticles from tea leaf extracts. Colloids Surf. B 173, 242–248 (2019)CrossRefGoogle Scholar
  12. 12.
    M. Chen, Y.G. Feng, X. Wang, T.C. Li, J.Y. Zhang, D.J. Qian, Silver nanoparticles capped by oleylamine: formation, growth, and self-organization. Langmuir 23, 5296–5304 (2007)PubMedCrossRefGoogle Scholar
  13. 13.
    C. Marambio-Jones, E.M.V. Hoek, A review of the antibacterial effects of silver nanomaterials and potential emplications for human health and the environment. J. Nanopart. Res. 12, 1531–1551 (2010)CrossRefGoogle Scholar
  14. 14.
    X. Dong, X. Ji, J. Jing, M. Li, J. Li, W. Yang, Synthesis of triangular silver nanoprisms by stepwise reduction of sodium borohydride and trisodium citrate. J. Phys. Chem. C 114, 2070–2074 (2010)CrossRefGoogle Scholar
  15. 15.
    Z. Shan, J. Wu, F. Xu, F.-Q. Huang, H. Ding, Highly effective silver/semiconductor photocatalytic composites prepared by a silver mirror reaction. J. Phys. Chem. C 112, 15423–15428 (2008)CrossRefGoogle Scholar
  16. 16.
    B. Pietrobon, M. McEachran, V. Kitaev, Synthesis of size-controlled faceted pentagonal silver nanorods with tunable plasmonic properties and self-assembly of these nanorods. ACS Nano 3, 21–26 (2009)PubMedCrossRefGoogle Scholar
  17. 17.
    B. Wiley, Y. Sun, Y. Xia, Synthesis of silver nanostructures with controlled shapes and properties. Acc. Chem. Res. 40, 1067–1076 (2007)PubMedCrossRefGoogle Scholar
  18. 18.
    W.R. Rolim, M.T. Pelegrino, B. de Araújo Lima, L.S. Ferraz, F.N. Costa, J.S. Bernardes, T. Rodigues, M. Brocchi, A.B. Seabra, Green tea extract mediated biogenic synthesis of silver nanoparticles: characterization, cytotoxicity evaluation and antibacterial activity. Appl. Surf. Sci. 463, 66–74 (2019)CrossRefGoogle Scholar
  19. 19.
    N. Durán, P.D. Marcato, M. Durán, A. Yadav, A. Gade, M. Rai, Mechanistic aspects in the biogenic synthesis of extracellular metal nanoparticles by peptides, bacteria, fungi, and plants. Appl. Microbiol. Biotechnol. 90, 1609–1624 (2011)PubMedCrossRefGoogle Scholar
  20. 20.
    N. Durán, A.B. Seabra, Metallic oxide nanoparticles: state of the art in biogenic syntheses and their mechanisms. Appl. Microbiol. Biotechnol. 95, 275–288 (2012)PubMedCrossRefGoogle Scholar
  21. 21.
    N. Durán, A.B. Seabra, Biogenic synthesized Ag/Au nanoparticles: production, characterization, and applications. Curr. Nanosci. 14, 82–94 (2018)Google Scholar
  22. 22.
    S. Davidović, V. Lazić, I. Vukoje, J. Papan, S.P. Anhrenkiel, S. Dimitrijević, J.M. Nedeljković, Dextran coated silver nanoparticles—chemical sensor for selective cysteine detection. Colloids Surf. B 160, 184–191 (2017)CrossRefGoogle Scholar
  23. 23.
    S. Pirtarighat, M. Ghannadnia, S. Baghshahi, Green synthesis of silver nanoparticles using the plant extract of Salvia spinosa grown in vitro and their antibacterial activity assessment. J. Nanostruct. Chem. 9, 1–9 (2019)CrossRefGoogle Scholar
  24. 24.
    M. Bhagat, R. Anand, R. Datt, V. Gupta, S. Arya, Green synthesis of silver nanoparticles using aqueous extract of Rosa brunonii Lindl and their morphological, biological and photocatalytic characterizations. J. Inorg. Organomet. Polym. 29, 1039–1047 (2019)CrossRefGoogle Scholar
  25. 25.
    M. Akter, M.M. Rahman, A.K.M.A. Ullah, M.T. Sikder, T. Hosokawa, T. Saito, M. Kurasaki, Brassica rapa var. japonica leaf extract mediated green synthesis of crystalline silver nanoparticles and evaluation of their stability, cytotoxicity and antibacterial activity. J. Inorg. Organomet. Polym. 28, 1483–1493 (2018)CrossRefGoogle Scholar
  26. 26.
    Y. Gavamukulya, E.N. Maina, A.M. Meroka, E.S. Madivoli, H.A. El-Shemy, F. Wamunyokoli, G. Magoma, Green synthesis and characterization of highly stable silver nanoparticles from ethanolic extracts of fruits of Annona muricata. J. Inorg. Organomet. Polym. (2019). CrossRefGoogle Scholar
  27. 27.
    L. Huang, Y. Sun, S. Mahmud, H. Liu, Biological and environmental applications of silver nanoparticles synthesized using the aqueous extract of Gingo biloba leaf. J. Inorg. Organomet. Polym. (2019). CrossRefGoogle Scholar
  28. 28.
    P. Velusamy, J. Das, R. Pachaiappan, B. Vaseeharan, K. Pandian, Greener approach for synthesis of antibacterial silver nanoparticles using aqueous solution of neem gum (Azadirachta indica L.). Ind. Crop. Prod. 66, 103–109 (2015)CrossRefGoogle Scholar
  29. 29.
    R. Sood, D.S. Chopra, Optimization of reaction conditions to fabricate Ocimum sanctum synthesized silver nanoparticles and its application to nano-gel systems for burn wounds. Mater. Sci. Eng. C 92, 575–589 (2018)CrossRefGoogle Scholar
  30. 30.
    R. Rajan, K. Chandran, S.L. Harper, S.-I. Yun, P.T. Kalaichelvan, Plant extract synthesized silver nanoparticles: an ongoing source of novel biocompatible materials. Ind. Crop. Prod. 70, 356–373 (2015)CrossRefGoogle Scholar
  31. 31.
    J.Y. Song, B.S. Kim, Rapid biological synthesis of silver nanoparticles using plant leaf extracts. Bioproc. Biosyst. Eng. 32, 79 (2008)CrossRefGoogle Scholar
  32. 32.
    S. Ahmed, M. Ahmad, B.L. Swami, S. Ikram, A review on plants extract mediated synthesis of silver nanoparticles for antimicrobial applications: a green expertise. J. Adv. Res. 7, 17–28 (2016)PubMedCrossRefGoogle Scholar
  33. 33.
    M. Milutinović, N. Radovanović, M. Rajilić-Stojanović, S. Šiler-Marinković, S. Dimitrijević, S. Dimitrijević-Branković, Microwave-assisted extraction for the recovery of antioxidants from waste Equisetum arvense. Ind. Crop. Prod. 61, 388–397 (2014)CrossRefGoogle Scholar
  34. 34.
    F.C.H.M. Do Monte, J.G. dos Santos, M. Russi, V.M.N. Bispo Lanziotti, L.K.A.M. Leal, G.M. de Andrade Cunha, Antinociceptive and anti-inflammatory properties of the hydroalcoholic extract of stems from Equisetum arvense L. in mice. Pharmacol. Res. 49, 239–243 (2004)PubMedCrossRefGoogle Scholar
  35. 35.
    N.S. Sandhu, S. Kaur, D. Chopra, Equietum arvense: pharmacology and phytochemistry—a review. Asian. J. Pharm. Clin. Res. 3, 146–150 (2010)Google Scholar
  36. 36.
    R. Stefanović, Paradigma održivog razvoja poljoprivrede - strateški koncept zaštite životne sredine. Ecologica 17, 112–114 (2010)Google Scholar
  37. 37.
    J.M. Čanadanović-Brunet, G.S. Ćetković, S.M. Djilas, V.T. Tumbas, S.S. Savatović, A.I. Mandić, S.L. Markov, D.D. Cvetković, Radical scavenging and antimicrobial activity of horsetail (Equisetum arvense L.) extracts. Int. J. Food Sci. Technol. 44, 269–278 (2009)CrossRefGoogle Scholar
  38. 38.
    K.P. Bankura, D. Maity, M.M.R. Mollick, D. Mondal, B. Bhowmick, M.K. Bain, A. Chakraborty, J. Sarkar, K. Acharya, D. Chattopadhyay, Synthesis, characterization and antimicrobial activity of dextran stabilized silver nanoparticles in aqueous medium. Carbohyd. Polym. 89, 1159–1165 (2012)CrossRefGoogle Scholar
  39. 39.
    J.M. Herrero-Martinez, M. Sanmartin, M. Roses, E. Bosch, C. Rafols, Determination of dissociation constants of flavonoids by capillary electrophoresis. Electrophoresis 26, 1886–1895 (2005)PubMedCrossRefGoogle Scholar
  40. 40.
    N. Sauerwald, M. Schwenk, J. Polster, E. Bengsch, Spectrometric pK determination of daphnetin, chlorogenic acid and quercetin. Zeitschrift fur naturforschung B 53(3), 315–321 (1998)CrossRefGoogle Scholar
  41. 41.
    K.L. Kelly, E. Coronado, L.L. Zhao, G.C. Schatz, The optical properties of metal nanoparticles: the influence of size, shape, and dielectric environment. J. Phys. Chem. B 107, 668–677 (2003)CrossRefGoogle Scholar
  42. 42.
    T. Huang, X.-H.N. Xu, Synthesis and characterization of tunable rainbow colored colloidal silver nanoparticles using single-nanoparticle plasmonic microscopy and spectroscopy. J. Mater. Chem. 20, 9867–9876 (2010)PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    P. Anbu, S.C.B. Gopinath, H.S. Yun, C.-G. Lee, Temperature-dependent green biosynthesis and characterization of silver nanoparticles using balloon flower plants and their antibacterial potential. J. Mol. Struct. 1177, 302–309 (2019)CrossRefGoogle Scholar
  44. 44.
    C.N. Lok, C.M. Ho, M. Chen, Q.Y. He, W.Y. Yu, H. Sun, P.K.H. Tam, J.F. Chiu, C.M. Che, Silver nanoparticles: partial oxidation and antibacterial activities. J. Biol. Inorg. Chem. 12, 527–534 (2007)PubMedCrossRefGoogle Scholar
  45. 45.
    J.R. Morones, J.L. Elechiguerra, A. Camacho, K. Holt, J.N. Kouri, J.T. Ramirez, M.J. Yacaman, The antibacterial effect of silver nanoparticles. Nanotechnology 16, 2346 (2005)PubMedCrossRefGoogle Scholar
  46. 46.
    Z.M. Xiu, J. Mao, P.J.J. Alvarez, Differential effect of common ligands and molecular oxygen on antimicrobial activity of silver nanoparticles versus silver ions. Environ. Sci. Technol. 45, 9003–9008 (2011)PubMedCrossRefGoogle Scholar
  47. 47.
    L. Wang, C. Hu, L. Shao, The antimicrobial activity of nanoparticles: present situation and prospects for the future. Int. J. Nanomed. 12, 1227–1249 (2017)CrossRefGoogle Scholar
  48. 48.
    D.H. Kim, J.C. Park, G.E. Jeon, C.S. Kim, J.H. Seo, Effect of the size and shape of silver nanoparticles on bacterial growth and metabolism by monitoring optical density and fluorescence intensity. Biotechnol. Bioproc. Eng. 22, 210–217 (2017)CrossRefGoogle Scholar
  49. 49.
    M.A. Raza, Z. Kanwal, A. Rauf, A.N. Sabri, S. Riaz, S. Naseem, Size- and shape-dependent antibacterial studies of silver nanoparticles synthesized by Wet chemical routes. Nanomaterials (Basel, Switzerland) 6, 74 (2016)CrossRefGoogle Scholar
  50. 50.
    I. Vukoje, E. Džunuzović, V. Vodnik, S. Dimitrijević, S.P. Ahrenkiel, J.M. Nedeljković, Synthesis, characterization, and antimicrobial activity of poly(GMA-co-EGDMA) polymer decorated with silver nanoparticles. J. Mater. Sci. 49, 6838–6844 (2014)CrossRefGoogle Scholar
  51. 51.
    I. Vukoje, E. Džunuzović, D. Lončarević, S. Dimitrijević, S.P. Ahrenkiel, J.M. Nedeljković, Synthesis, characterization, and antimicrobial activity of silver nanoparticles on poly(GMA-co-EGDMA) polymer support. Polym. Compos. 38, 1206–1214 (2017)CrossRefGoogle Scholar
  52. 52.
    V. Lazić, I. Smičiklas, J. Marković, D. Lončarević, J. Dostanić, S.P. Ahrenkiel, J.M. Nedeljković, Antibacterial ability of supported silver nanoparticles by functionalized hydroxyapatite with 5-aminosalicylic acid. Vacuum 148, 62–68 (2018)CrossRefGoogle Scholar
  53. 53.
    V. Lazić, K. Mihajlovski, A. Mraković, E. Illés, M. Stoiljković, S.P. Ahrenkiel, J.M. Nedeljković, Antimicrobial activity of silver nanoparticles supported by magnetite. ChemistrySelect 4, 4018–4024 (2019)CrossRefGoogle Scholar
  54. 54.
    C. Cattò, E. Garuglieri, L. Borruso, D. Erba, M.C. Casiraghi, F. Cappitelli, F. Villa, S. Zecchin, R. Zanchi, Impacts of dietary silver nanoparticles and probiotic administration on the microbiota of an in vitro gut model. Environ. Pollut. 245, 754–763 (2019)PubMedCrossRefGoogle Scholar
  55. 55.
    M. Panaček, R. Kolar, R. Večerova, J. Prucek, V. Soukupova, P. Kryštof, R. Hamal, L. Zboril, L. Kvitek, Antifungal activity of silver nanoparticles against Candida spp. Biomaterials 30, 6333–6340 (2009)PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Miona Miljković
    • 1
  • Vesna Lazić
    • 2
    Email author
  • Slađana Davidović
    • 1
  • Ana Milivojević
    • 3
  • Jelena Papan
    • 2
  • Margarida M. Fernandes
    • 4
    • 5
  • Senentxu Lanceros-Mendez
    • 6
    • 7
  • S. Phillip Ahrenkiel
    • 8
  • Jovan M. Nedeljković
    • 2
  1. 1.Department of Biochemical Engineering and Biotechnology, Faculty of Technology and MetallurgyUniversity of BelgradeBelgradeSerbia
  2. 2.Vinča Institute of Nuclear SciencesUniversity of BelgradeBelgradeSerbia
  3. 3.Department of Biochemical Engineering and Biotechnology, Center of Innovation, Faculty of Technology and MetallurgyUniversity of BelgradeBelgradeSerbia
  4. 4.Centre of PhysicsUniversity of MinhoBragaPortugal
  5. 5.Centre of Biological EngineeringUniversity of MinhoBragaPortugal
  6. 6.BCMaterials, Basque Center for Materials, Applications and Nanostructures, UPV/EHU Science ParkLeioaSpain
  7. 7.Ikerbasque, Basque Foundation for ScienceBilbaoSpain
  8. 8.South Dakota School of Mines and TechnologyRapid CityUSA

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