Skip to main content
SpringerLink
Log in

Antibacterial, anti-efflux, anti-biofilm, anti-slime (exopolysaccharide) production and urease inhibitory efficacies of novel synthesized gold nanoparticles coated Anthemis atropatana extract against multidrug- resistant Klebsiella pneumoniae strains

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

In this study, the antibacterial, anti-efflux, anti-biofilm, anti-slime (exopolysaccharide) production and urease inhibitory efficacies of green synthesized gold nanoparticles (AuNPs) coated Anthemis atropatana extract against multidrug- resistant (MDR) Klebsiella pneumoniae strains were evaluated. The green synthesized AuNPs were characterized by scanning electron microscopy (SEM), transmission electron microscopy (TEM), energy-dispersive X-ray spectroscopy (EDX), X-ray diffractometer (XRD), particle size distribution, zeta potential and Fourier-transform infrared spectroscopy (FTIR). Then, antibacterial, anti-slime (exopolysaccharide) production, anti-biofilm and anti-efflux activities of AuNPs were investigated using micro-dilation, Congored agar, microtiter plate and MIC of ethidium bromide methods, respectively. Subsequently, the expression of mrkA, wzm and acrB genes was evaluated using quantitative Real-Time PCR (qRT-PCR). The synthesized AuNPs exhibited antibacterial activity against MDR strains of K. pneumoniae (minimum inhibitory concentration (MIC) of 6.25–50 µg/ml), as well as showed significant anti-slime (exopolysaccharide) production, anti-biofilm and anti-efflux activities against MDR strains. AuNPs showed significant inhibition against jack-bean urease and down-regulated the expression of mrkA, wzm and acrB genes. Moreover, the in vitro cytotoxic activity confirmed by MTT assay on the HEK-293 normal cell line showed negligible cytotoxicity. Thus, the present study suggests the potential use of AuNPs in the development of novel therapeutics for the prevention of biofilm-associated K. pneumoniae 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

Similar content being viewed by others

References

  • Abhay K, Pandey M, Pooja S (2017) The Genus Anthemis: a 2012–2017 Literature review on chemical composition, antimicrobial, insecticidal and antioxidant activities of essential oils. Medicines (Basel) 4:68–75

    Google Scholar 

  • Alcántar-Curiel MD, Ledezma-Escalante CA, Jarillo-Quijada MD, Gayosso-Vázquez C, Morfín-Otero R, Rodríguez-Noriega E, Cedillo-Ramírez ML, Santos-Preciado JI, Girón JA (2018) Association of antibiotic resistance, cell adherence, and biofilm production with the endemicity of nosocomial Klebsiella pneumoniae. Biomed Res Int. https://doi.org/10.1155/2018/7012958

    Article  PubMed  PubMed Central  Google Scholar 

  • Ali SG, Ansari MA, Alzohairy MA, Alomary MN, AlYahya S, Jalal M, Khan HM, Asiri SMM, Ahmad W, Mahdi AA, El-Sherbeeny AM, El-Meligy MA (2020) Biogenic gold nanoparticles as potent antibacterial and antibiofilm nano-antibiotics against Pseudomonas aeruginosa. Antibiotics (Basel) 9:E100

    Article  Google Scholar 

  • Aslany S, Tafvizi F, Naseh V (2020) Characterization and evaluation of cytotoxic and apoptotic effects of green synthesis of silver nanoparticles using Artemisia Ciniformis on human gastric adenocarcinoma. Mater Today Commun 24:101011

    Article  CAS  Google Scholar 

  • Badeggi UM, Ismail E, Adeloye AO, Botha S, Badmus JA, Marnewick JL, Cupido CN, Hussein AA (2020) Green synthesis of gold nanoparticles capped with Procyanidins from Leucosidea sericea as potential antidiabetic and antioxidant agents. Biomolecules 10:E452

    Article  Google Scholar 

  • Chen T, Dong G, Zhang S, Zhang X, Zhao Y, Cao J, Zhou T, Wu Q (2020) Effects of iron on the growth, biofilm formation and virulence of Klebsiella pneumoniae causing liver abscess. BMC Microbiol 20:36–42

    Article  Google Scholar 

  • Cholley AC, Traoré O, Hennequin C, Aumeran C (2020) Klebsiella pneumoniae survival and regrowth in endoscope channel biofilm exposed to glutaraldehyde and desiccation. Eur J Clin Microbiol Infect Dis. https://doi.org/10.1007/s10096-020-03818-7

    Article  PubMed  Google Scholar 

  • de Oliveira Júnior NG, Franco OL (2020) Promising strategies for future treatment of Klebsiella pneumoniae biofilms. Future Microbiol 15:63–79

    Article  Google Scholar 

  • Dehghanizade S, Arasteh J, Mirzaie A (2018) Green synthesis of silver nanoparticles using Anthemis atropatana extract: characterization and in vitro biological activities. Artif. Cells. Nanomed. Biotechnol. 46:160–168

    Article  CAS  Google Scholar 

  • Del Pozo JL (2018) Biofilm-related disease. Expert Rev Anti Infect Ther 16:51–65

    Article  Google Scholar 

  • Delarampour A, Ghalehnoo ZR, Khademi F, Vaez H (2020) Antibiotic resistance patterns and prevalence of class I, II and III Integrons among clinical isolates of Klebsiella pneumoniae. Infez Med 28:64–69

    CAS  PubMed  Google Scholar 

  • Elbagory AM, Hussein AA, Meyer M (2019) The in vitro immunomodulatory effects of gold nanoparticles synthesized from Hypoxis hemerocallidea aqueous extract and hypoxoside on macrophage and natural killer cells. Int J Nanomedicine 14:9007–9018

    Article  Google Scholar 

  • Foroohimanjili F, Mirzaie A, Hamdi SMM, Noorbazargan H, Hedayati ChM, Dolatabadi A, Rezaie H, Bishak FM (2020) Antibacterial, antibiofilm, and antiquorum sensing activities of phytosynthesized silver nanoparticles fabricated from Mespilus germanica extract against multidrug resistance of Klebsiella pneumoniae clinical strains. J Microbiol 60:216–230

    CAS  Google Scholar 

  • Freeman DJ, Falkiner FR, Keane CT (1989) New method for detecting slime production by coagulase negative staphylococci. J Clin Pathol 42:872–874

    Article  CAS  Google Scholar 

  • Gabrielyan L, Trchounian A (2019) Antibacterial activities of transient metals nanoparticles and membranous mechanisms of action. World J Microbiol Biotechnol 35:162–175

    Article  Google Scholar 

  • Galdiero E, Di Onofrio V, Maione A, Gambino E, Gesuele R, Menale B, Ciaravolo M, Carraturo F, Guida M (2020) Allium ursinum and Allium oschaninii against Klebsiella pneumoniae and Candida albicans mono- and polymicrobic biofilms in in vitro static and dynamic models. Microorganisms 8:E336

    Article  Google Scholar 

  • Huang BC, Yi YC, Chang JS, Ng I (2019) Mechanism study of photo-induced gold nanoparticles formation by Shewanella oneidensis MR-1. Sci Rep 9:75–82

    Article  Google Scholar 

  • Ibrahim HM, Reda MM, Klingner A (2020) Preparation and characterization of green carboxymethylchitosan (CMCS)—polyvinyl alcohol (PVA) electrospun nanofibers containing gold nanoparticles (AuNPs) and its potential use as biomaterials. Int J Biol Macromol 151:821–829

    Article  CAS  Google Scholar 

  • Iram S, Hayat MQ, Tahir M, Gul A, Abdullah Ahmed I (2019) Chloroplast genome sequence of Artemisia scoparia: comparative analyses and screening of mutational hotspots. Plants (Basel) 8:E476

    Article  Google Scholar 

  • Jeyarani S, Vinita NM, Puja P, Senthamilselvi S, Devan U, Velangani AJ, Biruntha M, Pugazhendhi A, Kumar P (2020) Biomimetic gold nanoparticles for its cytotoxicity and biocompatibility evidenced by fluorescence-based assays in cancer (MDA-MB-231) and non-cancerous (HEK-293) cells. J Photochem Photobiol, B 202:111715. https://doi.org/10.1016/j.jphotobiol.2019.111715

    Article  CAS  Google Scholar 

  • Kafarski P, Talma M (2018) Recent advances in design of new urease inhibitors: a review. J Adv Res 13:101–112

    Article  CAS  Google Scholar 

  • Lee H, Lee DG (2018) Gold nanoparticles induce a reactive oxygen species-independent apoptotic pathway in Escherichia coli. Colloids Surf B Biointerfaces 167:1–7

    Article  Google Scholar 

  • Lee KX, Shameli K, Yew YP, Teow SY, Jahangirian H, Rafiee-Moghaddam R, Webster TJ (2020) Recent developments in the facile bio-synthesis of gold nanoparticles (AuNPs) and their biomedical applications. Int J Nanomed 15:275–300

    Article  Google Scholar 

  • Lenchenko E, Blumenkrants D, Sachivkina N, Shadrova N, Ibragimova A (2020) Morphological and adhesive properties of Klebsiella pneumoniae biofilms. Vet World 13:197–200

    Article  Google Scholar 

  • Malekjamshidi MR, Zandi H, Eftekhar F (2020) Prevalence of extended-spectrum β-lactamase and integron gene sarriage in multidrug-resistant Klebsiella species isolated from outpatients in Yazd, Iran. J Med Sci 45:23–31

    Google Scholar 

  • Manju S, Malaikozhundan B, Vijayakumar S, Shanthi S, Jaishabanu A, Ekambaram P, Vaseeharan B (2016) Antibacterial, antibiofilm and cytotoxic effects of Nigella sativa essential oil coated gold nanoparticles. Microb Pathog 91:129–135

    Article  CAS  Google Scholar 

  • Muthuchamy M, Govindan R, Shine K, Thangasamy V, Alharbi NS, Thillaichidambaram M, Khaled JM, Wen JL, Alanzi KF (2020) Anti-biofilm investigation of graphene/chitosan nanocomposites against biofilm producing P. aeruginosa and K. pneumoniae. Carbohydr Polym 230:115646. https://doi.org/10.1016/j.carbpol.2019.115646

    Article  CAS  PubMed  Google Scholar 

  • Nazer S, Andleeb S, Ali S, Gulzar N, Iqbal T, Khan MAR, Raza A (2019) Synergistic antibacterial efficacy of biogenic synthesized silver nanoparticles using Ajuga bractosa with standard antibiotics: a study against bacterial pathogens. Curr Pharm Biotechnol. https://doi.org/10.2174/1389201020666191001123219

    Article  Google Scholar 

  • Padilla E, Llobet E, Doménech-Sánchez A, Martínez-Martínez L (2010) Klebsiella pneumoniae AcrAB efflux pump contributes to antimicrobial resistance and virulence. Antimicrob Agents Chemother 54:177–183

    Article  CAS  Google Scholar 

  • Qian W, Wang W, Zhang J, Wang T, Liu M, Yang M, Sun Z, Li X, Li Y (2020) Antimicrobial and antibiofilm activities of ursolic acid against carbapenem-resistant Klebsiella pneumoniae. J. Antibiot (Tokyo). https://doi.org/10.1038/s41429-020-0285-6

    Article  PubMed  Google Scholar 

  • Qin X, Wu S, Hao M, Zhu J, Ding B, Yang Y, Xu X, Wang M, Yang F, Hu F (2020) The colonization of carbapenem-resistant Klebsiella pneumoniae: epidemiology, resistance mechanisms, and risk factors in patients admitted to intensive care units in China. J Infect Dis 221(Supplement_2):S206–S214

    Article  CAS  Google Scholar 

  • Rajkumari J, Meena H, Gangatharan M, Busi S (2017) Green synthesis of anisotropic gold nanoparticles using hordenine andt heir antibiofilm efficacy against Pseudomonas aeruginosa. IET Nanobiotechnol 11:987–994

    Article  Google Scholar 

  • Rumyantceva V, Rumyantceva V, Koshel E, Vinogradov V (2019) Biocide-conjugated magnetite nanoparticles as an advanced platform for biofilm treatment. Ther Deliv 10:241–250

    Article  CAS  Google Scholar 

  • Valsalam S, Agastian P, Esmail GA, Ghilan AM, Al-Dhabi NA, Arasu MV (2019) Biosynthesis of silver and gold nanoparticles using Musa acuminata colla flower and its pharmaceutical activity against bacteria and anticancer efficacy. J Photochem Photobiol, B 201:111670

    Article  CAS  Google Scholar 

  • Vuotto C, Longo F, Pascolini C, Donelli G (2017) Biofilm formation and antibiotic resistance in Klebsiella pneumoniae urinary strains. J Appl Microbiol 123:1003–1018

    Article  CAS  Google Scholar 

  • Wang Z, Huang X, Jin S, Wang H, Yuan L, Brash JL (2019) Rapid antibacterial effect of sunlight-exposed silicon nanowire arrays modified with Au/Ag alloy nanoparticles. J Mater Chem B 7:6202–6209

    Article  CAS  Google Scholar 

  • Xu X, Man L (2020) Papain mediated synthesized gold nanoparticles encore the potency of bioconjugated Flutamide. Curr Pharm Biotechnol. https://doi.org/10.2174/1389201021666200227121144

    Article  PubMed  Google Scholar 

  • Yael N, Slavin Jason A, Urs O, Häfeli Horacio B (2017) Metal nanoparticles: understanding the mechanisms behind antibacterial activity. J Nanobiotechnology 15:65–72

    Article  Google Scholar 

  • Yun Z, Chinnathambi A, Alharbi SA, Jin Z (2020) Biosynthesis of gold nanoparticles using Vetex negundo and evaluation of pro-apoptotic effect on human gastric cancer cell lines. J Photochem Photobiol B 203:111749

    Article  Google Scholar 

  • Zada S, Ahmad A, Khan S, Iqbal A, Ahmad S, Ali H, Fu P (2018) Biofabrication of gold nanoparticles by Lyptolyngbya JSC-1 extract as super reducing and stabilizing agents: synthesis, characterization and antibacterial activity. Microb Pathog 114:116–123

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Islamic Azad University (Roudehen Branch) for providing facilities to perform this work.

Author information

Authors and Affiliations

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

    Milad Khosravi, Amir Mirzaie & Aliasghar Bagheri Kashtali

  2. Department of Biotechnology, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Hassan Noorbazargan

Authors
  1. Milad Khosravi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amir Mirzaie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aliasghar Bagheri Kashtali
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hassan Noorbazargan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amir Mirzaie.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethics approval

Ethics approval for this study was obtained from Medical Branch and Islamic Azad University, Tehran, Iran permitted this study with number: IR.IAU. TMB.REC. 22.356.

Informed consent

Written informed consent was obtained from all patients participating in this study.

Additional information

Communicated by Erko Stackebrandt.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 7131 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khosravi, M., Mirzaie, A., Kashtali, A.B. et al. Antibacterial, anti-efflux, anti-biofilm, anti-slime (exopolysaccharide) production and urease inhibitory efficacies of novel synthesized gold nanoparticles coated Anthemis atropatana extract against multidrug- resistant Klebsiella pneumoniae strains. Arch Microbiol 202, 2105–2115 (2020). https://doi.org/10.1007/s00203-020-01930-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-020-01930-y

Keywords

Search

Navigation