Quinolone resistance genes (qnrA and qnrS) in bacteriophage particles from wastewater samples and the effect of inducing agents on packaged antibiotic resistance genes

Journal of Antimicrobial Chemotherapy

Volumn 69, Issue 5, 2014, Pages 1265-1274

  Colomer Lluch, Marta ^a   Jofre, Juan ^a   Muniesa, Maite ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

EDTA; Phages; Sodium citrate

Indexed keywords

BACTERIOPHAGE DNA; CIPROFLOXACIN; CITRATE SODIUM; EDETIC ACID; MITOMYCIN; RIVER WATER; ANTIINFECTIVE AGENT; QUINOLONE DERIVATIVE; VIRUS DNA; WASTE WATER;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; ENTEROBACTER CLOACAE; ESCHERICHIA COLI; FECES; GENE; GENETIC RESISTANCE; NONHUMAN; PREVALENCE; QNRA GENE; QNRS GENE; WASTE WATER; ANIMAL; BACTERIAL GENE; BACTERIOPHAGE; GENETICS; HORIZONTAL GENE TRANSFER; HUMAN; ISOLATION AND PURIFICATION; REAL TIME POLYMERASE CHAIN REACTION; VIROLOGY;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIOPHAGES; DNA, VIRAL; DRUG RESISTANCE, BACTERIAL; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; HUMANS; QUINOLONES; REAL-TIME POLYMERASE CHAIN REACTION; WASTE WATER;

EID: 84897940598     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkt528     Document Type: Article

References (41)

1. Herrera-León S, Gónzalez-Sanz R, Herrera-León L et al. Characterization of multidrug-resistant Enterobacteriaceae carrying plasmid-mediated quinolone resistance mechanisms in Spain. J Antimicrob Chemother 2010; 66: 287-90.
2. Ball P. Quinolone generations: natural history or natural selection? J Antimicrob Chemother 2000; 46 Suppl T1: 17-24.
3. Hooper DC. Emerging mechanisms of fluoroquinolone resistance. Emerg Infect Dis 2001; 7:337-341
4. Paterson DL. Resistance in gram-negative bacteria: Enterobacteriaceae. Am J Med 2006; 119 Suppl 1: S20-8.
5. Rodríguez-Martínez JM, Eliecer Cano M, Velasco C et al. Plasmid-mediated quinolone resistance: an update. J Infect Chemother 2011; 17: 149-82.
6. Martinez-Martinez L, Pascual A, Jacoby GA. Quinolone resistance from a transferable plasmid. Lancet 1998; 351: 797-9.
7. Nordmann P, Poirel L. Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J Antimicrob Chemother 2005; 56: 463-9.
8. Poirel L, Rodriguez-Martinez JM, Mammeri H et al. Origin of plasmid-mediated quinolone resistance determinant QnrA. Antimicrob Agents Chemother 2005; 49: 3523-5.
9. Robicsek A, Jacoby GA, Hooper DC. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis 2006; 6: 629-40.
10. Cambau E, Lascols C, Sougakoff W et al. Occurrence of qnrA-positive clinical isolates in French teaching hospitals during 2002-2005. Microbiol Infect 2006; 12: 1013-20.
11. Quiroga MP, Andres P, Petroni A et al. 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 2007; 51: 4466-70.
12. Poirel L, Cattoir V, Nordmann P. Plasmid-mediated quinolone resistance; interactions between human, animal and environmental ecologies. Front Microbiol 2012; 3: 24.
13. Zhang XX, Zhang T, Fang HH. Antibiotic resistance genes in water environment. Appl Microbiol Biotechnol 2009; 82: 397-414.
14. Muniesa M, García A, Miró E et al. Bacteriophages and diffusion of b-lactamase genes. Emerg Infect Dis 2004; 10: 1134-7.
15. Colomer-Lluch M, Jofre J, Muniesa M. Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS One 2011; 6: e17549.
16. Colomer-Lluch M, Imamovic L, Jofre J et al. Bacteriophages carrying antibiotic resistance genes in faecal waste from cattle, pigs, and poultry. Antimicrob Agents Chemother 2011; 55: 4908-11.
17. Minot S, Sinha R, Chen J et al. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res 2011; 21: 1616-25.
18. Taylor NG, Verner-Jeffreys DW, Baker-Austin C. Aquatic systems: maintaining, mixing and mobilising antimicrobial resistance? Trends Ecol Evol 2011; 26: 278-84.
19. Allen HK, Looft T, Bayles DO et al. Antibiotics in feed induce prophages in swine faecal microbiomes. MBio,2011;2:pii: e00260-11
20. Looft T, Johnson TA, Allen HK et al In-feed antibiotic effects on the swine intestinal microbiome. Proc Natl Acad Sci USA 2012; 109: 1691-6.
21. Lavilla S, Gonzá lez López JJ, Sabaté M et al. Prevalene of qnr genes among extended-spectrum b-lactamase-producing enterobacterial isolates in Barcelona, Spain. J Antimicrob Chemother 2008; 61: 291-5.
22. Livny J, Friedman DI. Characterizing spontaneous induction of Stx encoding phages using a selectable reporter system. Mol Microbiol 2004; 51: 1691-704.
23. Fuchs S, Mü hldorfer I, Donohue-Rolfe A et al. Influence of RecA on in vivo virulence and Shiga toxin 2 production in Escherichia coli pathogens. Microb Pathog 1999; 27: 13-23.
24. Meessen-Pinard M, Sekulovic O, Fortier LC. Evidence of in vivo prophage induction during Clostridium difficile infection. Appl Environ Microbiol 2012; 78: 7662-70.
25. Rolain JM, François P, Hernandez D et al. Genomic analysis of an emerging multiresistant Staphylococcus aureus strain rapidly spreading in cystic fibrosis patients revealed the presence of an antibiotic inducible bacteriophage. Biol Direct 2009; 4: 1.
26. Goerke C, Koller J,Wolz C. Ciprofloxacin and trimethoprim cause phage induction and virulence modulation in Staphylococcus aureus. Antimicrob Agents Chemother 2006; 50: 171-7.
27. Imamovic L, Muniesa M. Characterizing RecA-independent induction of Shiga toxin2-encoding phages by EDTA treatment. PLoS One 2012; 7: e32393.
28. ISO 10705-2 Water Quality-Detection and Enumeration of Bacteriophages-Part 2: Enumeration of Somatic Coliphages. Geneva, Switzerland: International Organization for Standardisation, 2000.
29. Allué-Guardia A, Imamovic L, Muniesa M. Evolution of a self-inducible cytolethal distending toxin type-V-encoding-bacteriophage from Escherichia coli O157:H7 to Shigella sonnei. J Virol, 2013 ;87:13665-75.
30. Standard Methods for the Examination of Water and Wastewater. 20th edn. Washington, DC: American Public Health Association, American Works Association and Water Environment Federation, 1998; 1200.
31. Imamovic L, Ballesté E, Jofre J et al. Quantification of Shiga toxin-converting bacteriophages in wastewater and in faecal samples by real-time quantitative PCR. Appl Environ Microbiol 2010; 76: 5693-701.
32. Edge TA, Hill S. Occurrence of antibiotic resistance in Escherichia coli from surface waters and faecal pollution sources near Hamilton, Ontario. Can J Microbiol 2005; 51: 501-5.
33. Schmieger H, Schicklmaier P. Transduction of multiple drug resistance of Salmonella enterica serovar Typhimurium DT104. FEMS Microbiol Lett 1999; 170: 251-6.
34. Witschel M, Egli T, Zehnder AJ et al. Transport of EDTA into cells of the EDTA-degrading bacterial strain DSM 9103. Microbiology 1999; 145: 973-83.
35. Vaara M. Agents that increase the permeability of the outer membrane. Microbiol Mol Biol Rev 1992; 56: 395-411.
36. Bury-Moné S, Nomane Y, Reymond N et al. Global analysis of extracytoplasmic stress signaling in Escherichia coli. PLoS Genet 2009; 5: e1000651.
37. Jackson EN, Laski F, Andres C. Bacteriophage P22 mutants that alter the specificity of DNA packaging. J Mol Biol 1982; 154: 551-63.
38. Modi SR, Lee HH, Spina CS et al. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 2013; 499: 219-22.
39. Heindorff K, Aurich O, Michaelis A et al. Genetic toxicology of ethylenediaminetetraacetic acid (EDTA). Mutat Res 1983; 115: 149-73.
40. Blanusa M, Varnai VM, Piasek M et al. Chelators as antidotes of metal toxicity: therapeutic and experimental aspects. Curr Med Chem 2005; 12: 2771-94.
41. Muniesa M, Colomer-Lluch M, Jofre J. Potential impact of environmental bacteriophages in spreading antibiotic resistance genes. Future Microbiol 2013; 8: 739-51.