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Evaluation the effect of ZnO nanoparticle derived Bacillus subtilis on the expression of efflux pump genes (AdeB AdeRS) in Acinetobacter baumannii

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Abstract

Purpose

Green approach to the nanoparticles, including metal oxides due to inevitable disadvantages of physical or chemical synthesis routes is attractive nowadays. Zink oxide (ZnO) nanoparticles play a key role in the medical and pharmaceutical fields. This research aimed to study the biologically synthesized ZnO nanoparticle using Bacillus subtilis, and evaluated its antibacterial properties.

Methods

Bacillus subtilis culture in a broth nutrient environment was used, followed by adding the Zinc acetate dehydrate. Biosynthesis of the nanoparticles was confirmed by the XRD, FTIR, and SEM imaging. The antibacterial effects of NPs on the expression of AdeB efflux pump genes and the AdeRS regulator were studied; clinical species of the Acinetobacter baumannii were collected from clinical samples of Khorramabad, using the phenotypic (MIC) and the genotypic methods through real-time PCR.

Results

X-ray diffraction pattern (XRD) result showed, that all of the peaks were related to the ZnO, and no other peaks were detected; it also demonstrated nanostructure nature with crystallite size of 25–50 nm. The results indicated, that the antibacterial properties of the nanoparticle increased the AdeRS expression and decreased the AdeB expression in 40% of the A. Baumannii. In addition, there was an increase in the AdeB expression in 60% of the species, indicating an increased probability for mutation.

Conclusion

Given the desirable inhibitory effects of biosynthesized ZnO NPs on the expression of AdeB and AdeRS, which play an important role in the pharmaceutical resistance of Acinetobacter species, it seems that ZnO NPs can be used as a medication candidate in pharmaceutical industry in the future.

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References

  1. Zarei, M., A. Jamnejad, and E. Khajehali, Antibacterial effect of silver nanoparticles against four foodborne pathogens. Jundishapur journal of microbiology, 2014. 7(1).

  2. Mohan S, et al. Biopolymers–application in nanoscience and nanotechnology. Recent advances in biopolymers. 2016;1(1):47–66.

    Google Scholar 

  3. Park E-J, Kim H, Kim Y, Yi J, Choi K, Park K. Inflammatory responses may be induced by a single intratracheal instillation of iron nanoparticles in mice. Toxicology. 2010;275(1–3):65–71.

    Article  CAS  Google Scholar 

  4. Chaloupka K, Malam Y, Seifalian AM. Nanosilver as a new generation of nanoproduct in biomedical applications. Trends Biotechnol. 2010;28(11):580–8.

    Article  CAS  Google Scholar 

  5. Babu Nagati V, et al. Green synthesis and characterization of silver nanoparticles from Cajanus cajan leaf extract and its antibacterial activity. Intl J Nanomater Biostruct. 2012;2(3):39–43.

    Google Scholar 

  6. Azari A, et al. Efficiency of magnitized graphene oxide nanoparticles in removal of 2, 4-dichlorophenol from aqueous solution. J Mazandaran Univ Med Sci. 2017;26(144):265–81.

    Google Scholar 

  7. Kiani A, Ahmadloo M, Shariatifar N, Moazzen M, Baghani AN, Khaniki GRJ, et al. Method development for determination of migrated phthalate acid esters from polyethylene terephthalate (PET) packaging into traditional Iranian drinking beverage (Doogh) samples: a novel approach of MSPE-GC/MS technique. Environ Sci Pollut Res. 2018;25(13):12728–38.

  8. Rachel, R., et al. Surface layers of ore-leaching Bacteria and Archaea. In EMC 2008 14th European Microscopy Congress 1–5 September 2008, Aachen, Germany. 2008. Springer.

  9. Gholami M, Shirzad-Siboni M, Yang J-K. Application of Ni-doped ZnO rods for the degradation of an azo dye from aqueous solutions. Korean J Chem Eng. 2016;33(3):812–22.

    Article  CAS  Google Scholar 

  10. Gharibzadeh F, Rezaei Kalantary R, Nasseri S, Esrafili A, Azari A. Reuse of polycyclic aromatic hydrocarbons (PAHs) contaminated soil washing effluent by bioaugmentation/biostimulation process. Sep Purif Technol. 2016;168:248–56.

    Article  CAS  Google Scholar 

  11. El Enshasy, H.A., et al., Medical and cosmetic applications of fungal nanotechnology: production, characterization, and bioactivity, in Fungal nanobionics: Principles and applications. 2018, Springer. p. 21–59.

  12. Mohammadi F, Esrafili A, Kermani M, Farzadkia M, Gholami M, Behbahani M. Application of amino modified mesostructured cellular foam as an efficient mesoporous sorbent for dispersive solid-phase extraction of atrazine from environmental water samples. Microchem J. 2019;146:753–62.

    Article  CAS  Google Scholar 

  13. Chokriwal A, Sharma MM, Singh A. Biological synthesis of nanoparticles using bacteria and their applications. Am J PharmTech Res. 2014;4(6):38–61.

    Google Scholar 

  14. Narayanan KB, Sakthivel N. Biological synthesis of metal nanoparticles by microbes. Adv Colloid Interf Sci. 2010;156(1–2):1–13.

    Article  CAS  Google Scholar 

  15. Azari A, et al. Nitrate removal from aqueous solution by carbon nanotubes magnetized with nano zero-valent iron. J Mazandaran Univ Med Sci. 2014;23(2):15–27.

    Google Scholar 

  16. Prasad K, Jha AK. ZnO nanoparticles: synthesis and adsorption study. Nat Sci. 2009;1(02):129.

    CAS  Google Scholar 

  17. Yunos a’b, M.Z., et al., Biosynthesis of zinc oxide nanoparticles by using fruits extracts of Ananas comosus and its antibacterial activity. 2019.

  18. Esmaeilzade, H., et al., the effect of zno nanoparticles on the growth of bacillus subtilis and Escherichia coli o157:h7. journal of food technology and nutrition, 2014. 11(3 (43)): p. -.

  19. Lin D, Xing B. Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ Pollut. 2007;150(2):243–50.

    Article  CAS  Google Scholar 

  20. Nabizadeh S, Shariatifar N, Shokoohi E, Shoeibi S, Gavahian M, Fakhri Y, et al. Prevalence and probabilistic health risk assessment of aflatoxins B 1, B 2, G 1, and G 2 in Iranian edible oils. Environ Sci Pollut Res. 2018;25(35):35562–70.

  21. Venkataraju JL, et al. Synthesis, characterization and evaluation of antimicrobial activity of zinc oxide nanoparticles. J Biochem Technol. 2014;3(5):151–4.

    Google Scholar 

  22. Nezamabadi V, et al. Biosynthesis and antibacterial activity of ZnO nanoparticles by Artemisia Aucheri extract. Iran J Biotechnol. 2020;18(2):82–91.

    Google Scholar 

  23. Gunalan S, Sivaraj R, Rajendran V. Green synthesized ZnO nanoparticles against bacterial and fungal pathogens. Prog Natural Sci Mater Intl. 2012;22(6):693–700.

    Article  Google Scholar 

  24. Tiwari V, et al. Mechanism of anti-bacterial activity of zinc oxide nanoparticle against Carbapenem-resistant Acinetobacter baumannii. Front Microbiol. 2018;9:1–10.

    Article  Google Scholar 

  25. Lin M-F, Lin YY, Tu CC, Lan CY. Distribution of different efflux pump genes in clinical isolates of multidrug-resistant Acinetobacter baumannii and their correlation with antimicrobial resistance. J Microbiol Immunol Infect. 2017;50(2):224–31.

    Article  CAS  Google Scholar 

  26. Khosrishahi N, Sharifi M. Isolation of carbapenem resistant Acinetobacter baumannii(CRAB) strains from patients and equipments of intensive care units (ICUs) at Qazvin between 2005-2006. Iranian J Med Microbiol. 2007;1(3):33–8.

    Google Scholar 

  27. Goudarzi H, et al. Functional analysis of multidrug efflux pumps genes of Acinetobacter baumannii strains. Pejouhesh dar Pezeshki (Research in Medicine). 2013;37(2):107–12.

    Google Scholar 

  28. Modarresi F, Azizi O, Shakibaie MR, Motamedifar M, Valibeigi B, Mansouri S. Effect of iron on expression of efflux pump (adeABC) and quorum sensing (luxI, luxR) genes in clinical isolates of Acinetobacter baumannii. Apmis. 2015;123(11):959–68.

    Article  CAS  Google Scholar 

  29. Behdad R, Pargol M, Mirzaie A, Karizi SZ, Noorbazargan H, Akbarzadeh I. Efflux pump inhibitory activity of biologically synthesized silver nanoparticles against multidrug-resistant Acinetobacter baumannii clinical isolates. J Basic Microbiol. 2020;60(6):494–507.

    Article  CAS  Google Scholar 

  30. Bouvet PJ, Grimont PA. Taxonomy of the genus Acinetobacter with the recognition of Acinetobacter baumannii sp. nov., Acinetobacter haemolyticus sp. nov., Acinetobacter johnsonii sp. nov., and Acinetobacter junii sp. nov. and emended descriptions of Acinetobacter calcoaceticus and Acinetobacter lwoffii. Int J Syst Evol Microbiol. 1986;36(2):228–40.

    CAS  Google Scholar 

  31. Constantiniu S, et al. Cultural and biochemical characteristics of Acinetobacter spp. strains isolated from hospital units. J Prevent Med. 2004;12(3–4):35–42.

    Google Scholar 

  32. Weinstein, M.P. and J.S. Lewis, The Clinical and Laboratory Standards Institute Subcommittee on Antimicrobial Susceptibility Testing: Background, Organization, Functions, and Processes. J Clin Microbiol, 2020. 58(3).

  33. Ali AA, et al. Green synthesis of ZnO nanoparticles using Bacillus subtilis and their catalytic performance in the one-pot synthesis of steroidal thiophenes. European Chemical Bulletin. 2014;3(9):939–45.

    Google Scholar 

  34. Wayne, P., Reference method for broth dilution antifungal susceptibility testing of yeasts, approved standard. CLSI document M27-A2, 2002.

  35. Ahmed SH, et al. Multidrug resistant Egyptian isolates of Acinetobacter baumannii. J Am Sci. 2011;7(1):1013–9.

    Google Scholar 

  36. Jassim KA, Ghaima KK, Saadedin SMK. AdeABC efflux pump genes in multidrug resistant Acinetobacter baumannii isolates. Avicenna J Clin Microbiol Infect. 2016;3(4):40898–8.

  37. Mahdi, Z.S., et al., Biosynthesis of Zinc Oxide Nano-rods Using Xanthomonas campestris. Biol. J. Microorg., 2017: p. 22.

  38. Jayaseelan C, Rahuman AA, Kirthi AV, Marimuthu S, Santhoshkumar T, Bagavan A, et al. Novel microbial route to synthesize ZnO nanoparticles using Aeromonas hydrophila and their activity against pathogenic bacteria and fungi. Spectrochim Acta A Mol Biomol Spectrosc. 2012;90:78–84.

  39. Mahdi ZS, Talebnia Roshan F, Nikzad M, Ezoji H. Biosynthesis of zinc oxide nanoparticles using bacteria: a study on the characterization and application for electrochemical determination of bisphenol A. Inorganic Nano-Metal Chem. 2020:1–9.

  40. Chang T-Y, Huang BJ, Sun JR, Perng CL, Chan MC, Yu CP, et al. AdeR protein regulates adeABC expression by binding to a direct-repeat motif in the intercistronic spacer. Microbiol Res. 2016;183:60–7.

  41. Peleg AY, Adams J, Paterson DL. Tigecycline efflux as a mechanism for nonsusceptibility in Acinetobacter baumannii. Antimicrob Agents Chemother. 2007;51(6):2065–9.

    Article  CAS  Google Scholar 

  42. Madhi, M., et al., Impact of chitosan and silver nanoparticles laden with antibiotics on multidrug-resistant Pseudomonas aeruginosa and Acinetobacter baumannii. Archives of Clinical Infectious Diseases, (In Press).

  43. Gupta D, Singh A, Khan AU. Nanoparticles as efflux pump and biofilm inhibitor to rejuvenate bactericidal effect of conventional antibiotics. Nanoscale Res Lett. 2017;12(1):1–6.

    Article  Google Scholar 

  44. Banoee M, et al. ZnO nanoparticles enhanced antibacterial activity of ciprofloxacin against Staphylococcus aureus and Escherichia coli. J Biomed Mater Res B Appl Biomater. 2010;93(2):557–61.

    Article  Google Scholar 

  45. Hornsey M, Ellington MJ, Doumith M, Thomas CP, Gordon NC, Wareham DW, et al. AdeABC-mediated efflux and tigecycline MICs for epidemic clones of Acinetobacter baumannii. J Antimicrob Chemother. 2010;65(8):1589–93.

  46. Coyne S, et al. Screening and quantification of the expression of antibiotic resistance genes in Acinetobacter baumannii with a microarray. Antimicrob Agents Chemother. 2010;54(1):333–40.

    Article  CAS  Google Scholar 

  47. Atasoy AR, Ciftci IH, Petek M, Terzi HA. Investigation of mutations in adeR and adeS gene regions in gentamicine resistant Acinetobacter baumannii isolates. Biotechnol Biotechnol Equip. 2016;30(2):360–7.

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank the head and staff of the Razi herbal medicines research center of Lorestan University of Medical Sciences.

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Correspondence to Farnaz Kheirandish.

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Saleh, F., Kheirandish, F., Hosseini, F. et al. Evaluation the effect of ZnO nanoparticle derived Bacillus subtilis on the expression of efflux pump genes (AdeB AdeRS) in Acinetobacter baumannii. J Environ Health Sci Engineer 19, 1133–1141 (2021). https://doi.org/10.1007/s40201-021-00679-w

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