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Biosynthesis of Fe3O4@Ag Nanocomposite and Evaluation of Its Performance on Expression of norA and norB Efflux Pump Genes in Ciprofloxacin-Resistant Staphylococcus aureus

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Abstract

At present, the universal health problem with Staphylococcus aureus is the emergence of multidrug-resistant strains due to the overuse of antibiotics. Drug extrusion through efflux pumps is one of the bacterial mechanisms to neutralize the bactericidal effect of antibiotics. The antibacterial activity of silver nanoparticle as well as Fe3O4 nanoparticle had been previously studied and widely described. Today, the development of green methods for nanomaterial synthesis is an important aspect of research in the field of nanotechnology. Here, we report the biosynthesis and characterization of Fe3O4@Ag nanocomposite by Spirulina platensis cyanobacterium and it impacts on the expression of efflux pump genes in ciprofloxacin-resistant S. aureus (CRSA). The physical properties of biosynthesized nanocomposite measured and confirmed by ultraviolet-visible spectroscopy, Fourier-transform infrared spectroscopy, X-ray diffraction, energy-dispersive X-ray spectroscopy, and scanning and transmission electron microscopy. The minimum inhibitory concentration (MIC) of ciprofloxacin in CRSA strains was determined in the presence of Fe3O4@Ag nanoparticles by broth microdilution method. The effect of Fe3O4@Ag nanocomposite on the expression of norA and norB genes was evaluated by real-time PCR. The physical analysis confirmed well-dispersed, highly stable, and mostly spherical Fe3O4/Ag NPs with the average size of 30–68 nm. The results of antibacterial tests showed the synergistic effects of nanocomposite and antibiotics in MIC reduction. Additionally, in the presence of Fe3O4@Ag nanocomposite, the expression of norA and norB genes was decreased more than twofold compared to control. In conclusion, the Fe3O4/Ag nanocomposite can use as an effective inhibitor of antibiotic resistance in medicine.

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References

  1. Lee Ventola C (2015) The antibiotic resistance crisis part 1: causes and threats. P T 40(4):277–283

    PubMed  PubMed Central  Google Scholar 

  2. Cosgrove SE (2006) The relationship between antimicrobial resistance and patient outcomes: mortality, length of hospital stay, and health care costs. Clin Infect Dis 15(42):S82–S89

    Article  Google Scholar 

  3. Sydnor ER, Perl TM (2011) Hospital epidemiology and infection control in acute-care settings. Clin Microbiol Rev 24(1):141–173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Wang L, Hu C, Shao L (2017) The antimicrobial activity of nanoparticles: present situation and prospects for the future. Int J Nanomedicine 12:1227–1249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Maleki Dizaj S, Lotfipour F, Barzegar-Jalali M, Zarrintana MH, Adibkia K (2014) Antimicrobial activity of the metals and metal oxide nanoparticles. Mater Sci Eng C 44:278–284

    Article  CAS  Google Scholar 

  6. Chen Y, Gao N, Jiang J (2013) Surface matters: enhanced bactericidal property of core–shell Ag–Fe2O3 nanostructures to their heteromer counterparts from one-pot synthesis. Small 9(19):3242–3246

    CAS  PubMed  Google Scholar 

  7. Gong P, He H, Li X, Wang K, Hu J, Tan W, Zhang S, Yang X (2007) Preparation and antibacterial activity of Fe3O4@Ag nanoparticles. Nanotechnology 18(28):285604

    Article  CAS  Google Scholar 

  8. Munita JM, Arias CA (2016) Mechanisms of antibiotic resistance. Microbiol Spectr 4(2):10

    Google Scholar 

  9. Jang S (2016) Multidrug efflux pumps in Staphylococcus aureus and their clinical implications. J Microbiol 54:1–8

    Article  CAS  PubMed  Google Scholar 

  10. Ubukata K, Itoh-Yamashita N, Konno M (1989) Cloning and expression of the norA gene for fluoroquinolone resistance in Staphylococcus aureus. Antimicrob Agents Chemother 33:1535–1539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Truong-Bolduc QC, Dunman PM, Strahilevitz J, Projan SJ, Hooper DC (2005) MgrA is a multiple regulator of two new efflux pumps in Staphylococcus aureus. J Bacteriol 187:2395–2405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Valenzuela R, Fuentes MC, Parra C, Baeza J, Duran N, Sharma SK, Knobel M, Freer J (2009) Influence of stirring velocity on the synthesis of magnetite nanoparticles (Fe3O4) by the co-precipitation method. J Alloys Compd 488(1):227–231

    Article  CAS  Google Scholar 

  13. CLSI (2018) Performance standards for antimicrobial susceptibility testing. 28th ed. CLSI supplement M100. Clinical and Laboratory Standards Institute, Wayne

  14. Ding Y, Onodera Y, Lee JC, Hooper DC (2008) NorB, an efflux pump in Staphylococcus aureus strain MW2, contributes to bacterial fitness in abscesses. J Bacteriol 190(21):7123–7129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wada M, Lkhagvadorj E, Bian L, Wang C, Chiba Y, Nagata S, Shimizu T, Yamashiro Y, Asahara T, Nomoto K (2010) Quantitative reverse transcription-PCR assay for the rapid detection of methicillin-resistant Staphylococcus aureus. J Appl Microbiol 108(3):779–788

    Article  CAS  PubMed  Google Scholar 

  16. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  17. Kooti M, Saiahi S, Motamedi H (2013) Fabrication of silver-coated cobalt ferrite nanocomposite and the study of its antibacterial activity. J Magn Magn Mater 333:138–143

    Article  CAS  Google Scholar 

  18. Ghazanfari M, Johar F, Yazdani A (2014) Synthesis and characterization of Fe3O4@ Ag core-shell: structural, morphological, and magnetic properties. J Ultrafine Grained Nanostruct Mater 47(2):97–103

    Google Scholar 

  19. Kooti M, Kharazi P, Motamedi H (2014) Preparation, characterization, and antibacterial activity of CoFe2O 4/polyaniline/Ag nanocomposite. J Taiwan Inst Chem E 45(5):2698–2704

    Article  CAS  Google Scholar 

  20. Buzoglu L, Maltas E, Ozmen M, Yildiz S (2014) Interaction of donepezil with human serum albumin on amine-modified magnetic nanoparticles. Colloid Surf A Physicochem Eng Asp 442:139–145

    Article  CAS  Google Scholar 

  21. Chandraker K, Nagwanshi R, Jadhav SK, Ghosh KK, Satnami ML (2017) Antibacterial properties of amino acid functionalized silver nanoparticles decorated on graphene oxide sheets. Spectrochim Acta A Mol Biomol Spectrosc 181:47–54

    Article  CAS  PubMed  Google Scholar 

  22. Sathyavathi R, Krishna MB, Rao SV, Saritha R, Rao DN (2010) Biosynthesis of silver nanoparticles using Coriandrum sativum leaf extract and their application in nonlinear optics. Adv Sci Lett 3(2):138–143

    Article  CAS  Google Scholar 

  23. Jain N, Bhargava A, Majumdar S, Tarafdar JC, Panwar J (2011) Extracellular biosynthesis and characterization of silver nanoparticles using Aspergillus flavus NJP08: a mechanism perspective. Nanoscale 3(2):635–641

    Article  CAS  PubMed  Google Scholar 

  24. Wijesekara I, Pangestuti R, Kim S-K (2011) Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohydr Polym 84(1):14–21

    Article  CAS  Google Scholar 

  25. Kurtan U, Guner A, Amir M, Baykal A (2017) Enhanced antibacterial performance of Fe3O4–Ag and MnFe2O4–Ag nanocomposites. Bull Mater Sci 40:147–155

    Article  CAS  Google Scholar 

  26. Hwang IS, Hwang JH, Choi H, Kim KJ, Lee DG (2012) Synergistic effects between silver nanoparticles and antibiotics and the mechanisms involved. J Med Microbiol 61(12):1719–1726

    Article  CAS  PubMed  Google Scholar 

  27. Costa SS, Falcão C, Viveiros M, Machado D, Martins M, Melo-Cristino J, Amaral L, Couto I (2011) Exploring the contribution of efflux on the resistance to fluoroquinolones in clinical isolates of Staphylococcus aureus. BMC Microbiol 11:241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Li XZ, Nikaido H (2009) Efflux-mediated drug resistance in bacteria: an update. Drugs 69:1555–1623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Gupta D, Singh A, Khan AU (2017) Nanoparticles as efflux pump and biofilm inhibitor to rejuvenate bactericidal effect of conventional antibiotics. Nanoscale Res Lett 12:454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Salehzadeh A, Hashemi Doulabi MS, Sohrabnia B, Jalali A (2018) The effect of thyme (Thymus vulgaris) extract on the expression of norA efflux pump gene in clinical strains of Staphylococcus aureus. J Genet Resour 4(1):26–36

    Google Scholar 

  31. Chen M, Feng YG, Wang X, Li TC, Zhang JY, Qian DJ (2007) Silver nanoparticles capped by oleylamine: formation, growth and self-organization. Langmuir 23:5296–5304

    Article  CAS  PubMed  Google Scholar 

  32. Patel V, Berthold D, Puranik P, Gantar M (2015) Screening of cyanobacteria and microalgae for their ability to synthesize silver nanoparticles with antibacterial activity. Biotechnol Rep 5:112–119

    Article  Google Scholar 

  33. Lengke MF, Fleet ME, Southam G (2007) Biosynthesis of silver nanoparticles by filamentous cyanobacteria from a silver (I) nitrate complex. Langmuir 23(5):2694–2699

    Article  CAS  PubMed  Google Scholar 

  34. Ramesh R, Geerthana M, Prabhu S, Sohila S (2017) Synthesis and characterization of the superparamagnetic Fe3O4/Ag nanocomposites. J Clust Sci 28:963–969

    Article  CAS  Google Scholar 

  35. Rai MK, Deshmukh SD, Ingle AP, Gade AK (2012) Silver nanoparticles: the powerful nanoweapon against multidrug-resistant bacteria. J Appl Microbiol 112(5):841–852

    Article  CAS  PubMed  Google Scholar 

  36. Shrivastava S, Bera T, Roy A, Singh G, Ramachandrarao P, Dash D (2007) Characterization of enhanced antibacterial effects of novel silver nanoparticles. Nanotech 18(22):225103

    Article  CAS  Google Scholar 

  37. Sharma VK, Yngard RA, Lin Y (2009) Silver nanoparticles: green synthesis and their antimicrobial activities. Adv Colloid Interf Sci 145:83–96

    Article  CAS  Google Scholar 

  38. Mohan YM, Lee K, Premkumar T, Geckeler KE (2007) Hydrogel networks as nanoreactors: a novel approach to silver nanoparticles for antibacterial applications. Polymer 48:158–164

    Article  CAS  Google Scholar 

  39. Wypij M, Czarnecka J, Świecimska M, Dahm H, Rai M, Golinska P (2018) Synthesis, characterization and evaluation of antimicrobial and cytotoxic activities of biogenic silver nanoparticles synthesized from Streptomyces xinghaiensis OF1 strain. World J Microbiol Biotechnol 34(2):23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Rasht Branch, Islamic Azad University, Rasht, Iran

    Nastaran Shokoofeh & Ali Salehzadeh

  2. Department of Chemistry, Faculty of Sciences, University of Guilan, P.O. Box 41335–1914, Rasht, Iran

    Zeinab Moradi-Shoeili

  3. Department of Biology, Faculty of Sciences, University of Guilan, Rasht, Iran

    Akram Sadat Naeemi

  4. Department of Biology, Faculty of Science, Arak University, Arak, Iran

    Amir Jalali

  5. Department of Cell and Molecular Biology, University of Guilan, Rasht, Iran

    Mohammad Hedayati

Authors
  1. Nastaran Shokoofeh
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  2. Zeinab Moradi-Shoeili
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  3. Akram Sadat Naeemi
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  4. Amir Jalali
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  5. Mohammad Hedayati
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  6. Ali Salehzadeh
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Correspondence to Ali Salehzadeh.

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Shokoofeh, N., Moradi-Shoeili, Z., Naeemi, A.S. et al. Biosynthesis of Fe3O4@Ag Nanocomposite and Evaluation of Its Performance on Expression of norA and norB Efflux Pump Genes in Ciprofloxacin-Resistant Staphylococcus aureus. Biol Trace Elem Res 191, 522–530 (2019). https://doi.org/10.1007/s12011-019-1632-y

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