Skip to main content

Advertisement

SpringerLink
Log in

Plasmid-Mediated Quinolone Resistance (PMQR) Genes and Class 1 Integrons in Quinolone-Resistant Marine Bacteria and Clinical Isolates of Escherichia coli from an Aquacultural Area

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Antimicrobial usage in aquaculture selects for antimicrobial-resistant microorganisms in the marine environment. The relevance of this selection to terrestrial animal and human health is unclear. Quinolone-resistance genes qnrA, qnrB, and qnrS were chromosomally located in four randomly chosen quinolone-resistant marine bacteria isolated from an aquacultural area with heavy quinolone usage. In quinolone-resistant uropathogenic clinical isolates of Escherichia coli from a coastal area bordering the same aquacultural region, qnrA was chromosomally located in two E. coli isolates, while qnrB and qnrS were located in small molecular weight plasmids in two other E. coli isolates. Three quinolone-resistant marine bacteria and three quinolone-resistant E. coli contained class 1 integrons but without physical association with PMQR genes. In both marine bacteria and uropathogenic E. coli, class 1 integrons had similar co-linear structures, identical gene cassettes, and similarities in their flanking regions. In a Marinobacter sp. marine isolate and in one E. coli clinical isolate, sequences immediately upstream of the qnrS gene were homologous to comparable sequences of numerous plasmid-located qnrS genes while downstream sequences were different. The observed commonality of quinolone resistance genes and integrons suggests that aquacultural use of antimicrobials might facilitate horizontal gene transfer between bacteria in diverse ecological locations.

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

Similar content being viewed by others

References

  1. Marshall BM, Levy SB (2011) Food animals and antimicrobials: impacts on human health Clin Microbiol Rev 24:718–733. doi:10.1128/CMR.00002-11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Domingues S, Harms K, Fricke WF, Johnsen PJ, Da Silva GJ, Nielsen KM (2012) Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species PLoS Pathog 8:e1002837. doi:10.1371/journal.ppat.1002837

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Cabello FC, Godfrey HP, Tomova A, Ivanova L, Dölz H, Millanao A, Buschmann AH (2013) Antimicrobial use in aquaculture re-examined: its relevance to antimicrobial resistance and to animal and human health Environ Microbiol 15:1917–1942. doi:10.1111/1462-2920.1213

    Article  PubMed  Google Scholar 

  4. Cabello FC, Godfrey HP, Buschmann AH, Dölz HJ (2016) Aquaculture as yet another environmental gateway to the development and globalisation of antimicrobial resistance Lancet Infect Dis 16:e127–e133. doi:10.1016/S1473-3099(16)00100-6

    Article  PubMed  Google Scholar 

  5. Prescott JF (2006) History of antimicrobial usage in agriculture. In: Aarestrup FM (ed) Antimicrobial resistance in bacteria of animal origin. ASM Press, Washington, D.C., pp. 19–27

    Google Scholar 

  6. Cantas L, Shah SQ, Cavaco LM, Manaia CM, Walsh F, Popowska M, Garelick H, Bürgmann H, Sørum H (2013) A brief multi-disciplinary review on antimicrobial resistance in medicine and its linkage to the global environmental microbiota Front Microbiol 4:96. doi:10.3389/fmicb.2013.00096

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Hastings PJ, Rosenberg SM, Slack A (2004) Antibiotic-induced lateral transfer of antibiotic resistance Trends Microbiol 12:401–404

    Article  PubMed  CAS  Google Scholar 

  8. Sun M, Chang Z, Van den Brink PJ, Li J, Zhao F, Rico A (2016) Environmental and human health risks of antimicrobials used in Fenneropenaeus chinensis aquaculture production in China Environ Sci Pollut Res Int 23:15689–15702. doi:10.1007/s11356-016-6733-y

    Article  PubMed  CAS  Google Scholar 

  9. Baharoglu Z, Mazel D (2011) Vibrio cholerae triggers SOS and mutagenesis in response to a wide range of antibiotics: a route towards multiresistance Antimicrob Agents Chemother 55:2438–2441. doi:10.1128/AAC.01549-10

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Shah SQ, Cabello FC, L'Abée-Lund TM, Tomova A, Godfrey HP, Buschmann AH, Sørum H (2014) Antimicrobial resistance and antimicrobial resistance genes in marine bacteria from salmon aquaculture and non-aquaculture sites Environ Microbiol 16:1310–1320. doi:10.1111/1462-2920.12421

    Article  PubMed  CAS  Google Scholar 

  11. Muziasari WI, Parnanen K, Johnson TA, Lyra C, Karkman A, Stedtfeld RD, Tamminen M, Tiedje JM, Virta M (2016) Aquaculture changes the profile of antibiotic resistance and mobile genetic element associated genes in Baltic Sea sediments FEMS Microbiol Ecol 92:fiw052. doi:10.1093/femsec/fiw052

    Article  PubMed  CAS  Google Scholar 

  12. Angulo FJ, Nargund VN, Chiller TC (2004) Evidence of an association between use of anti-microbial agents in food animals and anti-microbial resistance among bacteria isolated from humans and the human health consequences of such resistance J Vet Med B Infect Dis Vet Public Health 51:374–379

    Article  PubMed  CAS  Google Scholar 

  13. Love DC, Rodman S, Neff RA, Nachman KE (2011) Veterinary drug residues in seafood inspected by the European Union, United States, Canada, and Japan from 2000 to 2009 Environ Sci Technol 45:7232–7240. doi:10.1021/es201608q

    Article  PubMed  CAS  Google Scholar 

  14. Chen DQ, Yang L, Luo YT, Mao MJ, Lin YP, Wu AW (2013) Prevalence and characterization of quinolone resistance in Laribacter hongkongensis from grass carp and Chinese tiger frog J Med Microbiol 62:1559–1564. doi:10.1099/jmm.0.059451-0

    Article  PubMed  CAS  Google Scholar 

  15. Roy Chowdhury P, McKinnon J, Wyrsch E, Hammond JM, Charles IG, Djordjevic SP (2014) Genomic interplay in bacterial communities: implications for growth promoting practices in animal husbandry Front Microbiol 5:394. doi:10.3389/fmicb.2014.00394

    Article  PubMed  PubMed Central  Google Scholar 

  16. Deng YT, Wu YL, Tan AP, Huang YP, Jiang L, Xue HJ, Wang WL, Luo L, Zhao F (2014) Analysis of antimicrobial resistance genes in Aeromonas spp. isolated from cultured freshwater animals in China Microb Drug Resist 20:350–356. doi:10.1089/mdr.2013.0068

    Article  PubMed  CAS  Google Scholar 

  17. Hooper DC, Jacoby GA (2016) Topoisomerase inhibitors: fluoroquinolone mechanisms of action and resistance. Cold Spring Harb Perspect Med 6. doi:10.1101/cshperspect.a025320

  18. 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 

  19. Fonseca EL, Vicente AC (2013) Epidemiology of qnrVC alleles and emergence out of the Vibrionaceae family J Med Microbiol 62:1628–1630. doi:10.1099/jmm.0.062661-0

    Article  PubMed  Google Scholar 

  20. Kim HB, Wang M, Park CH, Kim EC, Jacoby GA, Hooper DC (2009) oqxAB encoding a multidrug efflux pump in human clinical isolates of Enterobacteriaceae Antimicrob Agents Chemother 53:3582–3584. doi:10.1128/AAC.01574-08

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Ma J, Zeng Z, Chen Z, Xu X, Wang X, Deng Y, Lü D, Huang L, Zhang Y, Liu J, Wang M (2009) High prevalence of plasmid-mediated quinolone resistance determinants qnr, aac(6′)-Ib-cr, and qepA among ceftiofur-resistant Enterobacteriaceae isolates from companion and food-producing animals Antimicrob Agents Chemother 53:519–524. doi:10.1128/AAC.00886-08

    Article  PubMed  CAS  Google Scholar 

  22. Nakaminami H, Noguchi N, Sasatsu M (2010) Fluoroquinolone efflux by the plasmid-mediated multidrug efflux pump QacB variant QacBIII in Staphylococcus aureus Antimicrob Agents Chemother 54:4107–4111. doi:10.1128/AAC.01065-09

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Rodríguez-Martínez JM, Diaz de Alba P, Briales A, Machuca J, Lossa M, Fernández-Cuenca F, Rodríguez Baño J, Martínez-Martínez L, Pascual Á (2013) Contribution of OqxAB efflux pumps to quinolone resistance in extended-spectrum-beta-lactamase-producing Klebsiella pneumoniae J Antimicrob Chemother 68:68–73. doi:10.1093/jac/dks377

    Article  PubMed  CAS  Google Scholar 

  24. Robicsek A, Strahilevitz J, Jacoby GA, Macielag M, Abbanat D, Park CH, Bush K, Hooper DC (2006) Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase Nat Med 12:83–88

    Article  PubMed  CAS  Google Scholar 

  25. Zhao JY, Dang H (2012) Coastal seawater bacteria harbor a large reservoir of plasmid-mediated quinolone resistance determinants in Jiaozhou Bay, China Microb Ecol 64:187–199. doi:10.1007/s00248-012-0008-z

    Article  PubMed  CAS  Google Scholar 

  26. Cesaro A, Bettoni RR, Lascols C, Merens A, Soussy CJ, Cambau E (2008) Low selection of topoisomerase mutants from strains of Escherichia coli harbouring plasmid-borne qnr genes J Antimicrob Chemother 61:1007–1015. doi:10.1093/jac/dkn077

    Article  PubMed  CAS  Google Scholar 

  27. Martínez-Martínez L, Cano ME, Rodríguez-Martìnez JM, Calvo J, Pascual A (2008) Plasmid-mediated quinolone resistance Expert Rev Anti-Infect Ther 6:685–711

    Article  PubMed  CAS  Google Scholar 

  28. Jakobsen L, Cattoir V, Jensen KS, Hammerum AM, Nordmann P, Frimodt-Møller N (2012) Impact of low-level fluoroquinolone resistance genes qnrA1, qnrB19 and qnrS1 on ciprofloxacin treatment of isogenic Escherichia coli strains in a murine urinary tract infection model J Antimicrob Chemother 67:2438–2444. doi:10.1093/jac/dks224

    Article  PubMed  CAS  Google Scholar 

  29. Domínguez-Herrera J, Velasco C, Docobo-Pérez F, Rodríguez-Martínez JM, López-Rojas R, Briales A, Pichardo C, Díaz-de-Alba P, Rodríguez-Baño J, Pascual A, Pachón J (2013) Impact of qnrA1, qnrB1 and qnrS1 on the efficacy of ciprofloxacin and levofloxacin in an experimental pneumonia model caused by Escherichia coli with or without the GyrA mutation Ser83Leu J Antimicrob Chemother 68:1609–1615. doi:10.1093/jac/dkt063

    Article  PubMed  CAS  Google Scholar 

  30. Michon A, Allou N, Chau F, Podglajen I, Fantin B, Cambau E (2011) Plasmidic qnrA3 enhances Escherichia coli fitness in absence of antibiotic exposure PLoS One 6:e24552. doi:10.1371/journal.pone.0024552

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Cattoir V, Nordmann P (2009) Plasmid-mediated quinolone resistance in gram-negative bacterial species: an update Curr Med Chem 16:1028–1046

    Article  PubMed  CAS  Google Scholar 

  32. Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A (2009) Plasmid-mediated quinolone resistance: a multifaceted threat Clin Microbiol Rev 22:664–689. doi:10.1128/microbiolspec.PLAS-0006-2013

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Nordmann P, Poirel L (2005) Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae J Antimicrob Chemother 56:463–469

    Article  PubMed  CAS  Google Scholar 

  34. Rosewarne CP, Pettigrove V, Stokes HW, Parsons YM (2010) Class 1 integrons in benthic bacterial communities: abundance, association with Tn402-like transposition modules and evidence for coselection with heavy-metal resistance FEMS Microbiol Ecol 72:35–46. doi:10.1111/j.1574-6941.2009.00823.x

    Article  PubMed  CAS  Google Scholar 

  35. Stokes HW, Gillings MR (2011) Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into gram-negative pathogens FEMS Microbiol Rev 35:790–819. doi:10.1111/j.1574-6976.2011.00273.x

    Article  PubMed  CAS  Google Scholar 

  36. Cattoir V, Poirel L, Mazel D, Soussy CJ, Nordmann P (2007) Vibrio splendidus as the source of plasmid-mediated QnrS-like quinolone resistance determinants Antimicrob Agents Chemother 51:2650–2651

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Cattoir V, Poirel L, Aubert C, Soussy CJ, Nordmann P (2008) Unexpected occurrence of plasmid-mediated quinolone resistance determinants in environmental Aeromonas spp Emerg Infect Dis 14:231–237. doi:10.3201/eid1402.070677

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Xia R, Guo X, Zhang Y, Xu H (2010) qnrVC-like gene located in a novel complex class 1 integron harboring the ISCR1 element in an Aeromonas punctata strain from an aquatic environment in Shandong Province, China Antimicrob Agents Chemother 54:3471–3474. doi:10.1128/AAC.01668-09

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Han JE, Kim JH, Choresca Jr CH, Shin SP, Jun JW, Chai JY, Park SC (2012) First description of ColE-type plasmid in Aeromonas spp. carrying quinolone resistance (qnrS2) gene Lett Appl Microbiol 55:290–294. doi:10.1111/j.1472-765X.2012.03293.x

    Article  PubMed  CAS  Google Scholar 

  40. Del Castillo CS, Hikima J, Jang HB, Nho SW, Jung TS, Wongtavatchai J, Kondo H, Hirono I, Takeyama H, Aoki T (2013) Comparative sequence analysis of a multidrug-resistant plasmid from Aeromonas hydrophila Antimicrob Agents Chemother 57:120–129. doi:10.1128/AAC.01239-12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Quiroga MP, Andres P, Petroni A, Soler Bistué AJ, Guerriero L, Vargas LJ, Zorreguieta A, Tokumoto M, Quiroga C, Tolmasky ME, Galas M, Centrón D (2007) Complex class 1 integrons with diverse variable regions, including aac(6′)-Ib-cr, and a novel allele, qnrB10, associated with ISCR1 in clinical enterobacterial isolates from Argentina Antimicrob Agents Chemother 51:4466–4470

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Chen YT, Liao TL, Liu YM, Lauderdale TL, Yan JJ, Tsai SF (2009) Mobilization of qnrB2 and ISCR1 in plasmids Antimicrob Agents Chemother 53:1235–1237. doi:10.1128/AAC.00970-08

    Article  PubMed  CAS  Google Scholar 

  43. Rodríguez-Martínez JM, Cano ME, Velasco C, Martínez-Martínez L, Pascual A (2011) Plasmid-mediated quinolone resistance: an update J Infect Chemother 17:149–182. doi:10.1007/s10156-010-0120-2

    Article  PubMed  CAS  Google Scholar 

  44. Buschmann AH, Tomova A, López A, Maldonado MA, Henríquez LA, Ivanova L, Moy F, Godfrey HP, Cabello FC (2012) Salmon aquaculture and antimicrobial resistance in the marine environment PLoS One 7:e42724. doi:10.1371/journal.pone

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Tomova A, Ivanova L, Buschmann AH, Rioseco ML, Kalsi RK, Godfrey HP, Cabello FC (2015) Antimicrobial resistance genes in marine bacteria and human uropathogenic Escherichia coli from a region of intensive aquaculture Environ Microbiol Rep 7:803–809. doi:10.1111/1758-2229.12327

    Article  PubMed  CAS  Google Scholar 

  46. Barton BM, Harding GP, Zuccarelli AJ (1995) A general method for detecting and sizing large plasmids Anal Biochem 226:235–240

    Article  PubMed  CAS  Google Scholar 

  47. Liu SL, Hessel A, Sanderson KE (1993) Genomic mapping with I-Ceu I, an intron-encoded endonuclease specific for genes for ribosomal RNA, in Salmonella spp., Escherichia coli, and other bacteria Proc Natl Acad Sci U S A 90:6874–6878

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Xu H, Davies J, Miao V (2007) Molecular characterization of class 3 integrons from Delftia spp J Bacteriol 189:6276–6283

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Song JS, Jang SJ, Lee JJ, Lee JH, Bae IK, Jeong BC, Cha SS, Lee JH, Hong SK, Lee SH (2010) Association of the bla CMY-10 gene with a novel complex class 1 integron carrying an ISCR1 element in clinical isolates from Korea Clin Microbiol Infect 16:1013–1017. doi:10.1111/j.1469-0691.2009.03002.x

    Article  PubMed  CAS  Google Scholar 

  50. Lévesque C, Piché L, Larose C, Roy PH (1995) PCR mapping of integrons reveals several bnovel combinations of resistance genes Antimicrob Agents Chemother 39:185–191

    Article  PubMed  PubMed Central  Google Scholar 

  51. Sunde M, Sørum H (1999) Characterization of integrons in Escherichia coli of the normal intestinal flora of swine Microb Drug Resist 5:279–287

    Article  PubMed  CAS  Google Scholar 

  52. Gaze WH, Abdouslam N, Hawkey PM, Wellington EM (2005) Incidence of class 1 integrons in a quaternary ammonium compound-polluted environment Antimicrob Agents Chemother 49:1802–1807

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Stalder T, Barraud O, Casellas M, Dagot C, Ploy MC (2012) Integron involvement in environmental spread of antibiotic resistance Front Microbiol 3:119. doi:10.3389/fmicb.2012.00119

    Article  PubMed  PubMed Central  Google Scholar 

  54. Poirel L, Liard A, Rodriguez-Martinez JM, Nordmann P (2005) Vibrionaceae as a possible source of Qnr-like quinolone resistance determinants J Antimicrob Chemother 56:1118–1121

    Article  PubMed  CAS  Google Scholar 

  55. Saga T, Kaku M, Onodera Y, Yamachika S, Sato K, Takase H (2005) Vibrio parahaemolyticus chromosomal qnr homologue VPA0095: demonstration by transformation with a mutated gene of its potential to reduce quinolone susceptibility in Escherichia coli Antimicrob Agents Chemother 49:2144–2145

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Gillings MR (2014) Integrons: past, present, and future Microbiol Mol Biol Rev 78:257–277. doi:10.1128/MMBR.00056-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Kehrenberg C, Friederichs S, de Jong A, Michael GB, Schwarz S (2006) Identification of the plasmid-borne quinolone resistance gene qnrS in Salmonella enterica serovar Infantis J Antimicrob Chemother 58:18–22

    Article  PubMed  CAS  Google Scholar 

  58. Karczmarczyk M, Stephan R, Hachler H, Fanning S (2012) Complete nucleotide sequence of pVQS1 containing a quinolone resistance determinant from Salmonella enterica serovar Virchow associated with foreign travel J Antimicrob Chemother 67:1861–1864. doi:10.1093/jac/dks158

    Article  PubMed  CAS  Google Scholar 

  59. Jensen RV, Depasquale SM, Harbolick EA, Hong T, Kernell AL, Kruchko DH, Modise T, Smith CE, McCarter LL, Stevens AM (2013) Complete genome sequence of prepandemic Vibrio parahaemolyticus BB22OP Genome Announc 1:e00002–e00012. doi:10.1128/genomeA.00002-12

    Article  PubMed  PubMed Central  Google Scholar 

  60. Aedo S, Ivanova L, Tomova A, Cabello FC (2014) Plasmid-related quinolone resistance determinants in epidemic Vibrio parahaemolyticus, uropathogenic Escherichia coli, and marine bacteria from an aquaculture area in Chile Microb Ecol 68:324–328. doi:10.1007/s00248-014-0409-2

    Article  PubMed  CAS  Google Scholar 

  61. Ramirez MS, Nikolaidis N, Tolmasky ME (2013) Rise and dissemination of aminoglycoside resistance: the aac(6′)-Ib paradigm Front Microbiol 4:121. doi:10.3389/fmicb.2013.00121

    Article  PubMed  PubMed Central  Google Scholar 

  62. Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA, Hooper DC (2006) qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States Antimicrob Agents Chemother 50:2872–2874

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Jacoby GA, Griffin CM, Hooper DC (2011) Citrobacter spp. as a source of qnrB alleles Antimicrob Agents Chemother 55:4979–4984. doi:10.1128/AAC.05187-11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Hatosy SM, Martiny AC (2015) The ocean as a global reservoir of antibiotic resistance genes Appl Environ Microbiol 81:7593–7599. doi:10.1128/AEM.00736-15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Ribeiro TG, Novais Â, Branquinho R, Machado E, Peixe L (2015) Phylogeny and comparative genomics unveil independent diversification trajectories of qnrB and genetic platforms within particular Citrobacter species Antimicrob Agents Chemother 59:5951–5958. doi:10.1128/AAC.00027-15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Lin M, Wu X, Yan Q, Ma Y, Huang L, Qin Y, Xu X (2016) Incidence of antimicrobial-resistance genes and integrons in antibiotic-resistant bacteria isolated from eels and aquaculture ponds Dis Aquat Org 120:115–123. doi:10.3354/dao03013

    Article  PubMed  CAS  Google Scholar 

  67. Guglielmini J, Quintais L, Garcillán-Barcia MP, de la Cruz F, Rocha EPC (2011) The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation PLoS Genet 7:e1002222. doi:10.1371/journal.pgen.1002222

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Silva J, Zemelman R, Mandoca MA, Henríquez M, Merino C, González C (1987) Antibiotic-resistant gram negative bacilli isolated from sea water and shellfish. Possible epidemiological implications Rev Latinoam Microbiol 29:165–169

    PubMed  CAS  Google Scholar 

  69. Miranda CD, Zemelman R (2001) Antibiotic resistant bacteria in fish from the Concepcion Bay, Chile Mar Pollut Bull 42:1096–1102

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Lenfest Ocean Program/Pew Charitable Trusts (FCC and AHB), Basal Program (FB001), Chile (AHB), and by a fellowship from the John Simon Guggenheim Foundation (FCC).

Author information

Authors and Affiliations

  1. Department of Microbiology and Immunology, New York Medical College, Valhalla, NY, USA

    Alexandra Tomova, Larisa Ivanova & Felipe C. Cabello

  2. Institute of Physiology, Faculty of Medicine, Comenius University in Bratislava, Bratislava, Slovakia

    Alexandra Tomova

  3. Centro i~mar and CeBiB, Universidad de Los Lagos, Puerto Montt, Chile

    Alejandro H. Buschmann

  4. Department of Pathology, New York Medical College, Valhalla, NY, USA

    Henry P. Godfrey

Authors
  1. Alexandra Tomova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Larisa Ivanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alejandro H. Buschmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Henry P. Godfrey
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Felipe C. Cabello
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Felipe C. Cabello.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tomova, A., Ivanova, L., Buschmann, A.H. et al. Plasmid-Mediated Quinolone Resistance (PMQR) Genes and Class 1 Integrons in Quinolone-Resistant Marine Bacteria and Clinical Isolates of Escherichia coli from an Aquacultural Area. Microb Ecol 75, 104–112 (2018). https://doi.org/10.1007/s00248-017-1016-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-017-1016-9

Keywords

Search

Navigation