Characterization of epidemic IncI1-Iγ plasmids harboring ambler class A and C genes in Escherichia coli and Salmonella enterica from animals and humans

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 9, 2015, Pages 5357-5365

  Smith, Hilde ^a   Bossers, Alex ^a   Harders, Frank ^a   Wu, Guanghui ^c   Woodford, Neil ^d   Schwarz, Stefan ^e   Guerra, Beatriz ^f   Rodríguez, Irene ^f,g   Van Essen Zandbergen, Alieda ^a   Brouwer, Michael ^a   Mevius, Dik ^a,b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c VETERINARY LABORATORIES AGENCY   (United Kingdom)

^d PUBLIC HEALTH ENGLAND   (United Kingdom)

^e FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^f FEDERAL INSTITUTE FOR RISK ASSESSMENT   (Germany)

^g HOSPITAL RAMÓN Y CAJAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE AMPC; BETA LACTAMASE CTX M; BETA LACTAMASE SHV; EXTENDED SPECTRUM BETA LACTAMASE; AMPC BETA-LACTAMASES; BACTERIAL PROTEIN; BETA LACTAMASE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM CONJUGATION; CELL DIVISION; CLADISTICS; COMPARATIVE STUDY; ESCHERICHIA COLI; GENETIC CODE; GENETIC VARIABILITY; HUMAN; INCI1 I GAMMA PLASMID; INHERITANCE; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHYLOGENETIC TREE; PRIORITY JOURNAL; RNA INTERFERENCE; SALMONELLA ENTERICA; ANIMAL; GENETICS; PHYLOGENY; PLASMID;

ANIMALS; BACTERIAL PROTEINS; BETA-LACTAMASES; ESCHERICHIA COLI; HUMANS; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; PLASMIDS; SALMONELLA ENTERICA;

EID: 84940906795     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.05006-14     Document Type: Article

References (52)

1. Carattoli A. 2008. Animal reservoirs for extended spectrum beta-lactamase producers. Clin Microbiol Infect 14(SUPPL. 1):S117-S123.
2. Ewers C, Bethe A, Semmler T, Guenther S, Wieler LH 2012. Extended-spectrum beta-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clin Microbiol Infect 18:646-655. http://dx.doi.org/10.1111/j.1469-0691.2012.03850.x.
3. Liebana E, Carattoli A, Coque TM, Hasman H, Magiorakos AP, Mevius D, Peixe L, Poirel L, Schuepbach-Regula G, Torneke K, Torren-Edo J, Torres C, Threlfall J. 2013. Public health risks of enterobacterial isolates producing extended-spectrum beta-lactamases or AmpC beta-lactamases in food and food-producing animals: an EU perspective of epidemiology, analytical methods, risk factors, and control options. Clin Infect Dis 56: 1030-1037. http://dx.doi.org/10.1093/cid/cis1043.
4. Carattoli A. 2011. Plasmids in Gram negatives: molecular typing of resistance plasmids. Int J Med Microbiol 301:654-658. http://dx.doi.org/10.1016/j.ijmm.2011.09.003.
5. CTX-M-1 in Salmonella enterica isolates from poultry and humans in France, 2003 to 2008. Antimicrob Agents Chemother 54: 4484-4486. http://dx.doi.org/10.1128/AAC.00460-10.
6. CTX-M-1 gene carried on an IncI1 plasmid in multidrug-resistant Salmonella enterica serovar Typhimurium DT104 in cattle in France. J Antimicrob Chemother 66:942-944. http://dx.doi.org/10.1093/jac/dkr014.
7. Carattoli A. 2013. Plasmids and the spread of resistance. Int J Med Microbiol 303:298-304. http://dx.doi.org/10.1016/j.ijmm.2013.02.001.
8. Dierikx C, van der Goot J, Fabri T, van Essen-Zandbergen A, Smith H, Mevius D. 2013. Extended-spectrum-beta-lactamase- and AmpC-beta-lactamase-producing Escherichia coli in Dutch broilers and broiler farmers. J Antimicrob Chemother 68:60-67. http://dx.doi.org/10.1093/jac/dks349.
9. Leverstein-van Hall MA, Dierikx CM, Cohen Stuart J, Voets GM, van den Munckhof MP, van Essen-Zandbergen A, Platteel T, Fluit AC, van de Sande-Bruinsma N, Scharinga J, Bonten MJ, Mevius DJ, National ESBL Study Group. 2011. Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect 17:873-880. http://dx.doi.org/10.1111/j.1469-0691.2011.03497.x.
10. Voets GM, Platteel TN, Fluit AC, Scharringa J, Schapendonk CM, Stuart JC, Bonten MJ, Hall MA, National ESBL Surveillance Working Group. 2012. Population distribution of beta-lactamase conferring resistance to third-generation cephalosporins in human clinical Enterobacteriaceae in the Netherlands. PLoS One 7:e52102. http://dx.doi.org/10.1371/journal.pone.0052102.
11. Woodford N, Ward ME, Kaufmann ME, Turton J, Fagan EJ, James D, Johnson AP, Pike R, Warner M, Cheasty T, Pearson A, Harry S, Leach JB, Loughrey A, Lowes JA, Warren RE, Livermore DM. 2004. Community and hospital spread of Escherichia coli producing CTX-M extended-spectrum beta-lactamases in the UK. J Antimicrob Chemother 54:735-743. http://dx.doi.org/10.1093/jac/dkh424.
12. CTX-M-15-carrying Escherichia coli and Salmonella isolates from livestock and food in Germany. J Antimicrob Chemother 69:2951-2958. http://dx.doi.org/10.1093/jac/dku270.
13. Garcia-Fernandez A, Chiaretto G, Bertini A, Villa L, Fortini D, Ricci A, Carattoli A. 2008. Multilocus sequence typing of IncI1 plasmids carrying extended-spectrum beta-lactamases in Escherichia coli and Salmonella of human and animal origin. J Antimicrob Chemother 61:1229-1233. http://dx.doi.org/10.1093/jac/dkn131.
14. Johnson TJ, Shepard SM, Rivet B, Danzeisen JL, Carattoli A. 2011. Comparative genomics and phylogeny of the IncI1 plasmids: a common plasmid type among porcine enterotoxigenic Escherichia coli. Plasmid 66: 144-151. http://dx.doi.org/10.1016/j.plasmid.2011.07.003.
15. Sampei G, Furuya N, Tachibana K, Saitou Y, Suzuki T, Mizobuchi K, Komano T. 2010. Complete genome sequence of the incompatibility group I1 plasmid R64. Plasmid 64:92-103. http://dx.doi.org/10.1016/j.plasmid.2010.05.005.
16. Wu G, Day MJ, Mafura MT, Nunez-Garcia J, Fenner JJ, Sharma M, van Essen-Zandbergen A, Rodriguez I, Dierikx C, Kadlec K, Schink AK, Wain J, Helmuth R, Guerra B, Schwarz S, Threlfall J, Woodward MJ, Woodford N, Coldham N, Mevius D. 2013. Comparative analysis of ESBL-positive Escherichia coli isolates from animals and humans from the UK, The Netherlands and Germany. PLoS One 8:e75392. http://dx.doi.org/10.1371/journal.pone.0075392.
17. van Essen-Zandbergen A, Smith H, Veldman K, Mevius D. 2007. Occurrence and characteristics of class 1, 2 and 3 integrons in Escherichia coli, Salmonella and Campylobacter spp. in the Netherlands J Antimicrob Chemother 59:746-750.
18. Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ 2005. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63:219-228. http://dx.doi.org/10.1016/j.mimet.2005.03.018.
19. Carattoli A. 2009. Resistance plasmid families in Enterobacteriaceae. Antimicrob Agents Chemother 53:2227-2238. http://dx.doi.org/10.1128/AAC.01707-08.
20. Dierikx CM, van Duijkeren E, Schoormans AH, van Essen-Zandbergen A, Veldman K, Kant A, Huijsdens XW, van der Zwaluw K, Wagenaar JA, Mevius DJ. 2012. Occurrence and characteristics of extended-spectrum-beta-lactamase- and AmpC-producing clinical isolates derived from companion animals and horses. J Antimicrob Chemother 67:1368-1374. http://dx.doi.org/10.1093/jac/dks049.
21. Sambook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
22. Barton BM, Harding GP, Zuccarelli AJ 1995. A general method for detecting and sizing large plasmids. Anal Biochem 226:235-240. http://dx.doi.org/10.1006/abio.1995.1220.
23. Brouwer MS, Bossers A, Harders F, van Essen-Zandbergen A, Mevius DJ, Smith HE. 2014. Complete genome sequences of IncI1 plasmids carrying extended-spectrum β-lactamase genes. Genome Announc 2(4): e00859-14. http://dx.doi.org/10.1128/genomeA.00859-14.
24. Besemer J, Lomsadze A, Borodovsky M. 2001. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 29:2607-2618.
25. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A. 2010. The Pfam protein families database. Nucleic Acids Res 38:D211-D222. http://dx.doi.org/10.1093/nar/gkp985.
26. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D, Bork P, Das U, Daugherty L, Duquenne L, Finn RD, Gough J, Haft D, Hulo N, Kahn D, Kelly E, Laugraud A, Letunic I, Lonsdale D, Lopez R, Madera M, Maslen J, McAnulla C, McDowall J, Mistry J, Mitchell A, Mulder N, Natale D, Orengo C, Quinn AF, Selengut JD, Sigrist CJ, Thimma M, Thomas PD, Valentin F, Wilson D, Wu CH, Yeats C. 2009. InterPro: the integrative protein signature database. Nucleic Acids Res 37:D211-D215. http://dx.doi.org/10.1093/nar/gkn785.
27. Gascuel O. 1997. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14:685-695. http://dx.doi.org/10.1093/oxfordjournals.molbev.a025808.
28. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL 2004. Versatile and open software for comparing large genomes. Genome Biol 5:R12. http://dx.doi.org/10.1186/gb-2004-5-2-r12.
29. Deloger M, El Karoui M, Petit MA 2009. A genomic distance based on MUM indicates discontinuity between most bacterial species and genera. J Bacteriol 191:91-99. http://dx.doi.org/10.1128/JB.01202-08.
30. Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254-267.
31. CMY plasmids and their possible role in source attribution of Salmonella enterica serotype Typhimurium infections. Foodborne Pathog Dis 11:301-306. http://dx.doi.org/10.1089/fpd.2013.1670.
32. Accogli M, Fortini D, Giufre M, Graziani C, Dolejska M, Carattoli A, Cerquetti M. 2013. IncI1 plasmids associated with the spread of CMY-2, CTX-M-1 and SHV-12 in Escherichia coli of animal and human origin. Clin Microbiol Infect 19:E238-E240. http://dx.doi.org/10.1111/1469-0691.12128.
33. CTX-M-1 gene in Escherichia coli from several animal species in France. J Antimicrob Chemother 67:3011-3012. http://dx.doi.org/10.1093/jac/dks308.
34. Mankovich JA, Hsu CH, Konisky J. 1986. DNA and amino acid sequence analysis of structural and immunity genes of colicins Ia and Ib. J Bacteriol 168:228-236.
35. Majeed H, Gillor O, Kerr B, Riley MA 2011. Competitive interactions in Escherichia colipopulations: the roleofbacteriocins. ISMEJ 5:71-81. http://dx.doi.org/10.1038/ismej.2010.90.
36. Takahashi H, Shao M, Furuya N, Komano T. 2011. The genome sequence of the incompatibility group Igamma plasmid R621a: evolution of IncI plasmids. Plasmid 66:112-121. http://dx.doi.org/10.1016/j.plasmid.2011.06.004.
37. Smet A, Van Nieuwerburgh F, Vandekerckhove TT, Martel A, Deforce D, Butaye P, Haesebrouck F. 2010. Complete nucleotide sequence of CTX-M-15-plasmids from clinical Escherichia coli isolates: insertional events of transposons and insertion sequences. PLoS One 5:e11202. http://dx.doi.org/10.1371/journal.pone.0011202.
38. Sakuma T, Tazumi S, Furuya N, Komano T. 2013. ExcA proteins of IncI1 plasmid R64 and IncIgamma plasmid R621a recognize different segments of their cognate TraY proteins in entry exclusion. Plasmid 69: 138-145. http://dx.doi.org/10.1016/j.plasmid.2012.11.004.
39. Furuya N, Komano T. 1994. Surface exclusion gene of IncI1 plasmid R64: nucleotide sequence and analysis of deletion mutants. Plasmid 32:80-84. http://dx.doi.org/10.1006/plas.1994.1047.
40. Wang J, Stephan R, Power K, Yan Q, Hachler H, Fanning S. 2014. Nucleotide sequences of 16 transmissible plasmids identified in nine multidrug-resistant Escherichia coli isolates expressing an ESBL phenotype isolated from food-producing animals and healthy humans. J Antimicrob Chemother 69:2658-2668. http://dx.doi.org/10.1093/jac/dku206.
41. Doumith M, Dhanji H, Ellington MJ, Hawkey P, Woodford N. 2012. Characterization of plasmids encoding extended-spectrum beta-lactamases and their addiction systems circulating among Escherichia coli clinical isolatesinthe UK.J Antimicrob Chemother 67:878-885. http://dx.doi.org/10.1093/jac/dkr553.
42. Mnif B, Vimont S, Boyd A, Bourit E, Picard B, Branger C, Denamur E, Arlet G. 2010. Molecular characterization of addiction systems of plasmids encoding extended-spectrum beta-lactamases in Escherichia coli. J Antimicrob Chemother 65:1599-1603. http://dx.doi.org/10.1093/jac/dkq181.
43. Christensen SK, Gerdes K. 2003. RelE toxins from bacteria and archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA. Mol Microbiol 48:1389-1400. http://dx.doi.org/10.1046/j.1365-2958.2003.03512.x.
44. Woodford N, Carattoli A, Karisik E, Underwood A, Ellington MJ, Livermore DM 2009. Complete nucleotide sequences of plasmids pEK204, pEK499, and pEK516, encoding CTX-M enzymes in three major Escherichia coli lineages from the United Kingdom, all belonging to the international O25:H4-ST131 clone. Antimicrob Agents Chemother 53: 4472-4482. http://dx.doi.org/10.1128/AAC.00688-09.
45. Komano T, Yoshida T, Narahara K, Furuya N. 2000. The transfer region of IncI1 plasmid R64: similarities between R64 tra and Legionella icm/dot genes. Mol Microbiol 35:1348-1359.
46. Gyohda A, Furuya N, Ishiwa A, Zhu S, Komano T. 2004. Structure and function of the shufflon in plasmid r64. Adv Biophys 38:183-213. http://dx.doi.org/10.1016/S0065-227X(04)80166-7.
47. Fricke WF, McDermott PF, Mammel MK, Zhao S, Johnson TJ, Rasko DA, Fedorka-Cray PJ, Pedroso A, Whichard JM, Leclerc JE, White DG, Cebula TA, Ravel J. 2009. Antimicrobial resistance-conferring plasmids with similarity to virulence plasmids from avian pathogenic Escherichia coli strains in Salmonella enterica serovar Kentucky isolates from poultry. Appl Environ Microbiol 75:5963-5971. http://dx.doi.org/10.1128/AEM.00786-09.
48. (CMY-2) among Salmonella and other Enterobacteriaceae. J Antimicrob Chemother 57:424-429. http://dx.doi.org/10.1093/jac/dki478.
49. Fricke WF, Wright MS, Lindell AH, Harkins DM, Baker-Austin C, Ravel J, Stepanauskas R. 2008. Insights into the environmental resistance gene pool from the genome sequence of the multidrug-resistant environmental isolate Escherichia coli SMS-3-5. J Bacteriol 190:6779-6794. http://dx.doi.org/10.1128/JB.00661-08.
50. Partridge SR. 2011. Analysis of antibiotic resistance regions in Gramnegative bacteria. FEMS Microbiol Rev 35:820-855. http://dx.doi.org/10.1111/j.1574-6976.2011.00277.x.
51. Bleicher A, Schofl G, Rodicio MD, Saluz HP 2013. The plasmidome of a Salmonella enterica serovar Derby isolated from pork meat. Plasmid 69:202-210. http://dx.doi.org/10.1016/j.plasmid.2013.01.001.
52. Richardson EJ, Limaye B, Inamdar H, Datta A, Manjari KS, Pullinger GD, Thomson NR, Joshi RR, Watson M, Stevens MP 2011. Genome sequences of Salmonella enterica serovar Typhimurium, Choleraesuis, Dublin, and Gallinarum strains of well-defined virulence in food-producing animals. J Bacteriol 193:3162-3163. http://dx.doi.org/10.1128/JB.00394-11.