Skip to main content

Advertisement

SpringerLink
Log in

Inhibitory Effect of Biosynthesized Silver Nanoparticles from Extract of Nitzschia palea Against Curli-Mediated Biofilm of Escherichia coli

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Extended spectrum beta lactamase (ESBL) are emerging beta-lactamases in Gram-negative pathogens, causing serious problems in hospitalized patients worldwide. Biofilm mode of virulence has decreased the efficiency of antibiotics used for treatment against ESBL pathogens. Therefore, there is an urgent need for alternative agents such as nanoparticles that can prevent and inhibit the biofilm formation. The aim of the present study was to inhibit the biofilm formed by ESBL-producing Escherichia coli using silver nanoparticles (AgNPs) synthesized with fresh water diatom (Nitzschia palea). AgNPs were characterized using UV-Vis spectroscopy, Fourier transform infrared (FTIR) spectroscopy, field emission scanning electron microscope (FESEM), energy-dispersive X-ray spectroscopy (EDX), and XRD. AgNPs at their biofilm inhibitory concentration (BIC) of 300 ng ml−1 significantly reduced the biofilm formed by E. coli. Interestingly, Congo red assay revealed the reduction of curli, essential for biofilm formation in the presence of AgNPs. Light and CLSM examination of the biofilm images also validated that in the presence of AgNPs, the biofilm architecture was disintegrated and the thickness was significantly reduced. Overall, the present study exemplifies the use of AgNPs as a plausible alternative for conventional coating agents on implant devices to prevent and control biofilm-associated urinary tract infections.

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

References

  1. Tenke, P., Kovacs, B., Jackel, M., & Nagy, E. (2006). The role of biofilm infection in urology. World Journal of Urology, 24, 13–20.

    Article  CAS  Google Scholar 

  2. Farajnia, S., Alikhani, M. Y., Ghotaslou, R., Naghili, B., & Nakhlband, A. (2009). Causative agents and antimicrobial susceptibilities of urinary tract infections in the northwest of Iran. International Journal of Infectious Diseases, 13, 140–144.

    Article  Google Scholar 

  3. Jacobsen, S. M., Stickler, D. J., Mobley, H. L., & Shirtliff, M. E. (2008). Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clinical Microbiology Reviews, 21, 26–59.

    Article  CAS  Google Scholar 

  4. Osthoff, M., McGuinness, S. L., Wagen, A. Z., & Eisen, D. P. (2015). Urinary tract infections due to extended-spectrum beta-lactamase-producing Gram-negative bacteria: identification of risk factors and outcome predictors in an Australian tertiary referral hospital. International Journal of Infectious Diseases, 34, 79–83.

    Article  Google Scholar 

  5. Pitout, J. D., & Laupland, K. B. (2008). Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. The Lancet Infectious Diseases, 8, 159–166.

    Article  CAS  Google Scholar 

  6. Dalgic, N., Sancar, M., Bayraktar, B., Dincer, E., & Pelit, S. (2011). Ertapenem for the treatment of urinary tract infections caused by extended-spectrum beta-lactamase-producing bacteria in children. Scandinavian Journal of Infectious Diseases, 43, 339–343.

    Article  CAS  Google Scholar 

  7. Evans, D. J., Allison, D. G., Brown, M. R., & Gilbert, P. (1991). Susceptibility of Pseudomonas eruginosa & Escherichia coli biofilms towards ciprofloxacin: effect of specific growth rate. The Journal of Antimicrobial Chemotherapy, 27, 177–184.

    Article  CAS  Google Scholar 

  8. Pages, J. M., James, C. E., & Winterhalter, M. (2008). The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria. Nature Reviews. Microbiology, 6, 893–903.

    Article  CAS  Google Scholar 

  9. Hasdemir, U. O., Chevalier, J., Nordmann, P., & Pages, J. M. (2004). Detection & prevalence of active drug efflux mechanism in various multidrug-resistant Klebsiella pneumoniae strains from Turkey. Journal of Clinical Microbiology, 42, 2701–2706.

    Article  CAS  Google Scholar 

  10. Ito, A., Taniuchi, A., May, T., Kawata, K., & Okabe, S. (2009). Increased antibiotic resistance of Escherichia coli in mature biofilms. Applied and Environmental Microbiology, 75, 4093–4100.

    Article  CAS  Google Scholar 

  11. Deep, A., Chaudhary, U., & Gupta, V. (2011). Quorum sensing and bacterial pathogenicity: from molecules to disease. J Lab Physicians, 3, 4–11.

    Article  CAS  Google Scholar 

  12. Brown, M. R., Allison, D. G., & Gilbert, P. (1988). Resistance of bacterial biofilms to antibiotics: a growth-rate related effect? The Journal of Antimicrobial Chemotherapy, 22, 777–780.

    Article  CAS  Google Scholar 

  13. Alves, M. J., Barreira, J. C., Carvalho, I., Trinta, L., Perreira, L., Ferreira, I. C., & Pintado, M. (2014). Propensity for biofilm formation by clinical isolates from urinary tract infections: developing a multifactorial predictive model to improve antibiotherapy. Journal of Medical Microbiology, 63, 471–477.

    Article  CAS  Google Scholar 

  14. Vuotto, C., Longo, F., Balice, M. P., Donelli, G., & Varaldo, P. E. (2014). Antibiotic resistance related to biofilm formation in Klebsiella pneumoniae. Pathogens, 3, 743–758.

    Article  CAS  Google Scholar 

  15. Bryers, J. D. (2008). Medical biofilms. Biotechnology and Bioengineering, 100, 1–18.

    Article  CAS  Google Scholar 

  16. Davey, M. E., & O'Toole, G. A. (2000). Microbial biofilms: from ecology to molecular genetics. Microbiology and Molecular Biology Reviews, 64, 847–867.

    Article  CAS  Google Scholar 

  17. Fisher, L. E., Hook, A. L., Ashraf, W., Yousef, A., Barrett, D. A., Scurr, D. J., Chen, X., Smith, E. F., Fay, M., Parmenter, C. D., Parkinson, R., & Bayston, R. (2015). Biomaterial modification of urinary catheters with antimicrobials to give long-term broadspectrum antibiofilm activity. Journal of Controlled Release, 202, 57–64.

    Article  CAS  Google Scholar 

  18. Hola, V., Ruzicka, F., & Horka, M. (2010). Microbial diversity in biofilm infections of the urinary tract with the use of sonication techniques. FEMS Immunology and Medical Microbiology, 59, 525–528.

    Article  CAS  Google Scholar 

  19. Berne, C., Ducret, A., Hardy, G. G., Brun, Y. V. (2015). Adhesins involved in attachment to abiotic surfaces by Gram-negative bacteria. Microbiology Spectrum, 3. doi:10.1128/microbiolspec.MB-0018-2015

  20. Kim, S. M., Lee, H. W., Choi, Y. W., Kim, S. H., Lee, J. C., Lee, Y. C., Seol, S. Y., Cho, D. T., & Kim, J. (2012). Involvement of curli fimbriae in the biofilm formation of Enterobacter cloacae. Journal of Microbiology, 50, 175–178.

    Article  CAS  Google Scholar 

  21. Dueholm, M. S., Albertsen, M., Otzen, D., & Nielsen, P. H. (2012). Curli functional amyloid systems are phylogenetically widespread & display large diversity in operon & protein structure. PloS One, 7, e51274.

    Article  CAS  Google Scholar 

  22. Kikuchi, T., Mizunoe, Y., Takade, A., Naito, S., & Yoshida, S. (2005). Curli fibers are required for development of biofilm architecture in Escherichia coli K-12 and enhance bacterial adherence to human uroepithelial cells. Microbiology and Immunology, 49, 875–884.

    Article  CAS  Google Scholar 

  23. Malloy, A. M., & Campos, J. M. (2011). Extended-spectrum beta-lactamases: a brief clinical update. The Pediatric Infectious Disease Journal, 30, 1092–1093.

    Article  Google Scholar 

  24. James, C. W., & Gurk-Turner, C. (2001). Cross-reactivity of beta-lactam antibiotics. Proc (Bayl Univ Med Cent), 14, 106–107.

    CAS  Google Scholar 

  25. Kanj, S. S., & Kanafani, Z. A. (2011). Current concepts in antimicrobial therapy against resistant gram-negative organisms: extended-spectrum beta-lactamase-producing Enterobacteriaceae, carbapenem-resistant Enterobacteriaceae, and multidrug-resistant Pseudomonas aeruginosa. Mayo Clinic Proceedings, 86, 250–259.

    Article  Google Scholar 

  26. MubarakAli, D., Thajuddin, N., Jeganathan, K., & Gunasekaran, M. (2011). Plant extract mediated synthesis of silver and gold nanoparticles and its antibacterial activity against clinically isolated pathogens. Colloids and Surfaces. B, Biointerfaces, 85, 360–365.

    Article  CAS  Google Scholar 

  27. Priyadarshini, S., Gopinath, V., Meera Priyadharsshini, N., MubarakAli, D., & Velusamy, P. (2012). Synthesis of anisotropic silver nanoparticles using novel strain, Bacillus flexus and its biomedical application. Colloids and Surfaces. B, Biointerfaces, 102, 232–237.

    Article  Google Scholar 

  28. Pugazhendhi, S., Sathya, P., Palanisamy, P. K., & Gopalakrishnan, R. (2016). Synthesis of silver nanoparticles through green approach using Dioscorea alata and their characterization on antibacterial activities and optical limiting behavior. Journal of Photochemistry and Photobiology. B, 159, 155–160.

    Article  CAS  Google Scholar 

  29. Eid, M., & Araby, E. (2013). Bactericidal effect of poly(acrylamide/itaconic acid)-silver nanoparticles synthesized by gamma irradiation against Pseudomonas aeruginosa. Applied Biochemistry and Biotechnology, 171, 469–487.

    Article  CAS  Google Scholar 

  30. Selvaraj, M., Pandurangan, P., Ramasami, N., Rajendran, S. B., Sangilimuthu, S. N., & Perumal, P. (2014). Highly potential antifungal activity of quantum-sized silver nanoparticles against Candida albicans. Applied Biochemistry and Biotechnology, 173, 55–66.

    Article  CAS  Google Scholar 

  31. Kumar, D. A., Palanichamy, V., & Roopan, S. M. (2014). Green synthesis of silver nanoparticles using Alternanthera dentata leaf extract at room temperature & their antimicrobial activity. Spectrochimica Acta. Part A, Molecular and Biomolecular Spectroscopy, 127, 168–171.

    Article  CAS  Google Scholar 

  32. Ansari, M. A., Khan, H. M., Khan, A. A., Cameotra, S. S., Saquib, Q., & Musarrat, J. (2014). Gum arabic capped-silver nanoparticles inhibit biofilm formation by multi-drug resistant strains of Pseudomonas aeruginosa. Journal of Basic Microbiology, 54, 688–699.

    Article  CAS  Google Scholar 

  33. Bhainsa, K. C., & D'Souza, S. F. (2006). Extracellular biosynthesis of silver nanoparticles using the fungus Aspergillus fumigatus. Colloids and Surfaces. B, Biointerfaces, 47, 160–164.

    Article  CAS  Google Scholar 

  34. Mandal, D., Kumar Dash, S., Das, B., Chattopadhyay, S., Ghosh, T., Das, D., & Roy, S. (2016). Bio-fabricated silver nanoparticles preferentially targets Gram positive depending on cell surface charge. Biomedicine & Pharmacotherapy, 83, 548–558.

    Article  CAS  Google Scholar 

  35. de Morais, M. G., Vaz Bda, S., de Morais, E. G., & Costa, J. A. (2015). Biologically active metabolites synthesized by microalgae. BioMed Research International, 2015, 835761.

    Google Scholar 

  36. Shanab, S. M., Mostafa, S. S., Shalaby, E. A., & Mahmoud, G. I. (2013). Aqueous extracts of microalgae exhibit antioxidant and anticancer activities. Asian Pac J Trop Biomed, 2, 608–615.

    Article  Google Scholar 

  37. Jena, J., Pradhan, N., Dash, B. P., Panda, P. K., & Mishra, B. K. (2014). Pigment mediated biogenic synthesis of silver nanoparticles using diatom Amphora sp. and its antimicrobial activity. Journal of Saudi Chemical Society, 19, 661–666.

    Article  Google Scholar 

  38. Mohseniazar, M., Barin, M., Zarredar, H., Alizadeh, S., & Shanehbandi, D. (2011). Potential of microalgae and lactobacilli in biosynthesis of silver nanoparticles. BioImpacts: BI, 1, 149–152.

    CAS  Google Scholar 

  39. Rajamanickam, K., Sudha, S. S., Francis, M., Sowmya, T., Rengaramanujam, J., Sivalingam, P., & Prabakar, K. (2013). Microalgae associated Brevundimonas sp. MSK 4 as the nano particle synthesizing unit to produce antimicrobial silver nanoparticles. Spectrochimica Acta. Part A, Molecular and Biomolecular Spectroscopy, 113, 10–14.

    Article  CAS  Google Scholar 

  40. Sudha, S. S., Rajamanickam, K., & Rengaramanujam, J. (2013). Microalgae mediated synthesis of silver nanoparticles and their antibacterial activity against pathogenic bacteria. Indian Journal of Experimental Biology, 51, 393–399.

    CAS  Google Scholar 

  41. Vijay, P., David, B., Pravin, P., & Miroslav, G. (2015). Screening of cyanobacteria and microalgae for their ability to synthesize silver nanoparticles with antibacterial activity. Biotechnology Rep, 5, 112–119.

    Article  Google Scholar 

  42. Hameed, A. S., Karthikeyan, C., Ahamed, A. P., Thajuddin, N., Alharbi, N. S., Alharbi, S. A., & Ravi, G. (2016). In vitro antibacterial activity of ZnO and Nd doped ZnO nanoparticles against ESBL producing Escherichia coli and Klebsiella pneumoniae. Scientific Reports, 6, 24312.

    Article  CAS  Google Scholar 

  43. Shafreen, R. M., Srinivasan, S., Manisankar, P., & Pandian, S. K. (2011). Biofilm formation by Streptococcus pyogenes: modulation of exopolysaccharide by fluoroquinolone derivatives. Journal of Bioscience and Bioengineering, 112, 345–350.

    Article  CAS  Google Scholar 

  44. Nithyanand, P., Beema Shafreen, R. M., Muthamil, S., & Karutha Pandian, S. (2015). Usnic acid, a lichen secondary metabolite inhibits Group A Streptococcus biofilms. Antonie Van Leeuwenhoek, 107, 263–272.

    Article  CAS  Google Scholar 

Download references

Acknowledgement

The financial support provided by UGC F.4-2/2006 (BSR)/BL/13-14/0151 in the form of Dr. D. S. Kothari Postdoctoral Fellow to RMBS is gratefully acknowledged. The instrumentation facility provided by the Department of Science and Technology, Government of India, through YSS-SERB [File No.SR YSS/20 l4/000127] is gratefully acknowledged. The authors kindly acknowledge the Department of Science and Technology (DST), New Delhi, India, for providing CLSM facility under DST-PURSE scheme (Ref. No: SR/FT/LS-113/2009). The author N.T. thanks the Deanship of Scientific Research, College of Science Research Centre, King Saud University, Kingdom of Saudi Arabia for supporting the work.

Author information

Authors and Affiliations

  1. Molecular Nanomedicine Research Unit, Centre for Nanoscience and Nanotechnology, Sathyabama University, Chennai, 600119, India

    Rajamohamed Beema Shafreen & Siddharthan Seema

  2. Division of Microbial Biodiversity and Bioenergy, Department of Microbiology, Bharathidasan University, Tiruchirappalli, Tamil Nadu, 600024, India

    Rajamohamed Beema Shafreen, Siddharthan Seema, Abdulazees Parveez Ahamed & Nooruddin Thajuddin

  3. Department of Botany and Microbiology, College of Science, King Saud University, 11451, Riyadh, Saudi Arabia

    Sulaiman Ali Alharbi

Authors
  1. Rajamohamed Beema Shafreen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Siddharthan Seema
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Abdulazees Parveez Ahamed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nooruddin Thajuddin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sulaiman Ali Alharbi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Rajamohamed Beema Shafreen or Nooruddin Thajuddin.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Supplementary Fig. 1

A and B represents the light and CLSM microscopy images of N. palea. C) Fully grown biomass of N. palea with F/2 medium in a closed type system was harvested and lyophilised. D) The dried powder of N. palea was further used for green synthesis of silver nanoparticles (JPEG 45 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shafreen, R.B., Seema, S., Ahamed, A.P. et al. Inhibitory Effect of Biosynthesized Silver Nanoparticles from Extract of Nitzschia palea Against Curli-Mediated Biofilm of Escherichia coli . Appl Biochem Biotechnol 183, 1351–1361 (2017). https://doi.org/10.1007/s12010-017-2503-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-017-2503-7

Keywords

Search

Navigation