Skip to main content

Advertisement

SpringerLink
Log in

Characterization of the complete sequences and stability of plasmids carrying the genes aac(6′)-Ib-cr or qnrS in Shigella flexneri in the Hangzhou area of China

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The aim of this study was to explore the fluoroquinolone resistance mechanism of aac (6′)-Ib-cr and qnrS gene by comparing complete sequences and stability of the aac(6′)-Ib-cr- and qnrS-positive plasmids from Shigella isolates in the Hangzhou area of China. The complete sequences of four newly acquired plasmids carrying aac(6′)-Ib-cr or qnrS were compared with those of two plasmids obtained previously and two similar reference Escherichia coli plasmids. The results showed that the length, antibiotic resistance genes and genetic environment were different among the plasmids. Moreover, the plasmid stability of three wild-type isolates and five plasmid transformants carrying aac(6′)-Ib-cr and/or qnrS was measured in vitro, and all eight isolates were found to have lost their aac(6′)-Ib-cr- or qnrS-positive plasmids to a different extent at different stages. When the plasmids were electroporated into Shigella flexneri or they lost positive plasmids, the MICs of ciprofloxacin increased or decreased two- to eightfold for aac(6′)-Ib-cr-positive plasmids and 16- to 32-fold for qnrS-positive plasmids. To our knowledge, this is the first report comparing the complete sequences and describing stability for the aac(6′)-Ib-cr- and qnrS-positive plasmids from Shigella isolates.

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

Similar content being viewed by others

References

  • Briales A, Rodríguez-Martínez JM, Velasco C, Díaz de Alba P, Domínguez-Herrera J, Pachón J, Pascual A (2011) In vitro effect of qnrA1, qnrB1, and qnrS1 genes on fluoroquinolone activity against isogenic Escherichia coli isolates with mutations in gyrA and parC. Antimicrob Agents Chemother 55:1266–1269

    Article  PubMed  CAS  Google Scholar 

  • Clinical and Laboratory Standards Institute (2018) Performance standards for antimicrobial susceptibility testing: 15th informational supplement: CLSI document M100, 28th. Wayne

  • Dutta S, Kawamura Y, Ezaki T, Nair GB, Iida K, Yoshida S (2005) Alteration in the gyrA subunit of DNA gyrase and the parC subunit of topoisomerase IV in quinolone-resistant Shigella dysenteriaee serotype 1 clinical isolates from Kolkata, India. Antimicrob Agents Chemother 49:1660–1661

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ferjani S, Saidani M, Amine FS, Boutiba Boubake (2015) Prevalence and characterization of plasmid-mediated quinolone resistance genes in extended-spectrum β-lactamase-producing Enterobacteriaceae in a Tunisian hospital. Microb Drug Resist 21:158–166

    Article  PubMed  CAS  Google Scholar 

  • Hata M, Suzuki M, Matsumoto M, Takahashi M, Sato K, Ibe S, Sakae K (2005) Cloning of a novel gene for quinolone resistance from a transferable plasmid in Shigella flexneri 2b. Antimicrob Agents Chemother 49:801–803

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hayes F (2000) The horizontal gene pool—bacterial plasmids and gene spread. Harwood Acad 86:251–252

    Google Scholar 

  • Herrera-León S, González-Sanz R, Herrera-León L, Echeita MA (2011) Characterization of multidrug-resistant Enterobacteriaceae carrying plasmid-mediated quinolone resistance mechanisms in Spain. J Antimicrob Chemother 66:287–290

    Article  PubMed  CAS  Google Scholar 

  • Huang SY, Dai L, Xia LN, Du XD, Qi YH, Liu HB, Wu CM, Shen JZ (2009) Increased prevalence of plasmid-mediated quinolone resistance determinants in chicken Escherichia coli isolates from 2001 to 2007. Foodborne Pathog Dis 6:1203–1209

    Article  PubMed  CAS  Google Scholar 

  • Jiang Y, Zhou Z, Qian Y, Wei Z, Yu Y, Hu S, Li L (2008) Plasmid-mediated quinolone resistance determinants qnr and aac(6′)-Ib-cr in extended-spectrum -lactamase-producing Escherichia coli and Klebsiella pneumoniae in China. J Antimicrob Chemother 61:1003–1006

    Article  PubMed  CAS  Google Scholar 

  • Kiiru J, Kariuki S, Goddeeris BM, Revathi G, Maina TW, Ndegwa DW, Muyodi J, Butaye P (2011) Escherichia coli strains from Kenyan patients carrying conjugatively transferable broad-spectrum β-lactamase. qnr, aac(6′)-Ib-cr and 16S rRNA methyltransferase genes. J Antimicrob Chemother 66:1639–1642

    Article  PubMed  CAS  Google Scholar 

  • Kim ES, Jeong J-Y, Jun J-B, Choi S-H, Lee S-O, Kim M-N, Woo JH, Kim YS (2009) Prevalence of aac(6′)-Ib-cr encoding a ciprofloxacin-modifying enzyme among Enterobacteriaceae blood isolates in Korea. Antimicrob Agents Chemother 53:2643–2645

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Machuca J, Briales A, Labrador G, Díaz-de-Alba P, López-Rojas R, Docobo-Pérez F, Martínez-Martínez L, Rodríguez-Baño J, Pachón ME, Pascual A, Rodríguez-Martínez JM (2014) Interplay between plasmid-mediated and chromosomal-mediated fluoroquinolone resistance and bacterial fitness in Escherichia coli. J Antimicrob Chemother 69:3203–3215

    Article  PubMed  CAS  Google Scholar 

  • Machuca J, Ortiz M, Recacha E, Díaz-De-Alba P, Docobo-Perez F, Rodríguez-Martínez JM, Pascual Á (2016) Impact of aac(6′)-Ib-cr in combination with chromosomal-mediated mechanisms on clinical quinolone resistance in Escherichia coli. J Antimicrob Chemother 71:3066–3071

    Article  PubMed  CAS  Google Scholar 

  • Margaritis A, Galani I, Chatzikonstantinou M, Petrikkos G, Souli M (2017) Plasmid-mediated quinolone resistance determinants among Gram-negative bacteraemia isolates: a hidden threat. J Med Microbiol 66:266–275

    Article  PubMed  Google Scholar 

  • Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, Edwards RA, Gerdes S, Parrello B, Shukla M, Vonstein V, Wattam AR, Xia F, Stevens R (2014) The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 42:D206–D214

    Article  PubMed  CAS  Google Scholar 

  • Park CH, Robicsek A, Jacoby GA, Sahm D, Hooper DC (2006) Prevalence in the United States of aac(6′)-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Chemother 50:3953–3955

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pu XY, Pan JC, Wang HQ, Zhang W, Huang ZC, Gu YM (2009) Characterization of fluoroquinolone-resistant Shigella flexneri in Hangzhou area of China. J Antimicrob Chemother 63:917–920

    Article  PubMed  CAS  Google Scholar 

  • Pu XY, Zhang Q, Pan JC, Shen Z, Zhang W (2013) Spontaneous mutation frequency and molecular mechanisms of Shigella flexneri fluoroquinolone resistance under antibiotic selective stress. World J Microbiol Biotechnol 29:365–371

    Article  PubMed  CAS  Google Scholar 

  • Pu XY, Pan JC, Zhang W, Zheng W, Wang HQ, Gu YM (2015) Quinolone resistance-determining region mutations and the plasmid-mediated quinolone resistance gene qnrS played important roles in decreased susceptibility to fluoroquinolones among Shigella isolates in southeast China between 1998 and 2013. Int J Antimicrob Agents 45:438–439

    Article  PubMed  CAS  Google Scholar 

  • Pu XY, Pan JC, Gu YM, Zheng W, Li J, Yu H (2016) Complete sequences and characterization of two novel plasmids carrying aac(6′)-Ib-cr and qnrS gene in Shigella flexneri. Microbial Drug Resistance 22:115–122

    Article  PubMed  CAS  Google Scholar 

  • Robicsek A, Jacoby GA, Hooper DC (2006) The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis 6:629–640

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Martínez JM, Machuca J, Cano ME, Calvo J, Martínez-Martínez L, Pascual A (2016) Plasmid-mediated quinolone resistance: two decades on. Drug Resist Updates 29:13–29

    Article  Google Scholar 

  • Ruiz J, Pons MJ, Gomes C (2012) Transferable mechanisms of quinolone resistance. Int J Antimicrob Agents 40:196–203

    Article  PubMed  CAS  Google Scholar 

  • Sambrook JS, Russell DW (2002) Molecular cloning, a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Shigemura K, Tanaka K, Yamamichi F, Shirakawa T, Miyake H, Fujisawa M (2012) Does mutation in gyrA and/or parC or efflux pump expression play the main role in fluoroquinolone resistance in Escherichia coli urinary tract infections?: A statistical analysis study. Int J Antimicrob Agents 40:516–520

    Article  PubMed  CAS  Google Scholar 

  • Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A (2009) Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 22:664–689

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sun H, Li S, Xie Z, Yang F, Sun Y, Zhu Y, Zhao X, Jiang S (2012) A novel multidrug resistance plasmid isolated from an Escherichia coli strain resistant to aminoglycosides. J Antimicrob Chemother 67:1635–1638

    Article  PubMed  CAS  Google Scholar 

  • Thong KL, Ngoi ST, Chai LC, Teh CS (2016) Quinolone resistance mechanisms among Salmonella enterica in Malaysia. Microb Drug Resist 22:259–272

    Article  PubMed  CAS  Google Scholar 

  • Xue G, Li J, Feng Y, Xu W, Li S, Yan C, Zhao H, Sun H (2017) High prevalence of plasmid-mediated quinolone resistance determinants in Escherichia coli and Klebsiella pneumoniae isolates from pediatric patients in China. Microb Drug Resist 23:107–114

    Article  PubMed  CAS  Google Scholar 

  • Yang H, Chen H, Yang Q, Chen M, Wang H (2008) High prevalence of plasmid-mediated quinolone resistance genes qnr and aac(6′)-Ib-cr in clinical isolates of Enterobacteriaceae from nine teaching hospitals in China. Antimicrob Agents Chemother 52:4268–4273

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang H, Duan G, Zhu J, Zhang W, Xi Y, Fan Q (2013) Prevalence and characterisation of plasmid-mediated quinolone resistance and mutations in the gyrase and topoisomerase IV genes among Shigella isolates from Henan, China, between 2001 and 2008. Int J Antimicrob Agents 42:173–177

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (No. 81301466) and the National Science Foundation of Zhejiang Province (No. LY15H160068).

Author information

Authors and Affiliations

  1. School of Medicine, Hangzhou Normal University, Hangzhou, 310036, Zhejiang, China

    Xiao-Ying Pu & Zhe Lu

  2. Department of Primary Health Care, Health and Family Planning Commission of Zhejiang Province, Hangzhou, 310006, Zhejiang, China

    Yaming Gu

  3. Hangzhou Center for Disease Control and Prevention, Hangzhou, 310021, Zhejiang, China

    Jun Li & Shu-Juan Song

Authors
  1. Xiao-Ying Pu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yaming Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shu-Juan Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhe Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiao-Ying Pu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pu, XY., Gu, Y., Li, J. et al. Characterization of the complete sequences and stability of plasmids carrying the genes aac(6′)-Ib-cr or qnrS in Shigella flexneri in the Hangzhou area of China. World J Microbiol Biotechnol 34, 72 (2018). https://doi.org/10.1007/s11274-018-2454-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-018-2454-3

Keywords

Search

Navigation