Comparative genomics of multidrug resistance-encoding incA/C plasmids from commensal and pathogenic escherichia coli from multiple animal sources

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Fernández Alarcón, Claudia ^a   Singer, Randall S ^a,b   Johnson, Timothy J ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAMASE; FLORFENICOL; TETRACYCLINE; ANTIINFECTIVE AGENT; ANTIPORTER; BACTERIAL PROTEIN; BETA LACTAMASE CMY 2; BETA-LACTAMASE CMY-2; DRUG DERIVATIVE; ESCHERICHIA COLI PROTEIN; FLOR PROTEIN, E COLI; TETA PROTEIN, BACTERIA; THIAMPHENICOL;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIUM ISOLATE; BETA LACTAMASE CMY 2 GENE; COMPARATIVE STUDY; CONTROLLED STUDY; DAIRY CATTLE; DNA BASE COMPOSITION; ESCHERICHIA COLI; FLOR GENE; GENETIC DIFFERENCE; GENOME ANALYSIS; HORIZONTAL GENE TRANSFER; MULTIDRUG RESISTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; SALMONELLA; SEQUENCE ANALYSIS; STRAB GENE; SWINE; TETA GENE; TETAR GENE; TURKEY (BIRD); ANIMAL; ANTIBIOTIC RESISTANCE; CATTLE; CHILE; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; ESCHERICHIA COLI INFECTION; GENE ORDER; GENETICS; GENOMICS; HUMAN; METHODOLOGY; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; UNITED STATES;

ANIMALIA; BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE; ESCHERICHIA COLI; SALMONELLA; SUIDAE;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIPORTERS; BACTERIAL PROTEINS; BETA-LACTAMASES; CATTLE; CHILE; CLUSTER ANALYSIS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; GENE ORDER; GENE TRANSFER, HORIZONTAL; GENOMICS; HUMANS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMIDS; SEQUENCE ANALYSIS, DNA; SWINE; TETRACYCLINE RESISTANCE; THIAMPHENICOL; TURKEYS; UNITED STATES;

EID: 80051630584     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023415     Document Type: Article

References (62)

1. McIntosh D, Cunningham M, Ji B, Fekete FA, Parry EM, et al. (2008) Transferable, multiple antibiotic and mercury resistance in Atlantic Canadian isolates of Aeromonas salmonicida subsp. salmonicida is associated with carriage of an IncA/C plasmid similar to the Salmonella enterica plasmid pSN254. J Antimicrob Chemother 61: 1221-1228.
2. Norman A, Hansen LH, She QX, Sorensen SJ, (2008) Nucleotide sequence of pOLA52: A conjugative IncX1 plasmid from Escherichia coli which enables biofilm formation and multidrug efflux. Plasmid 60: 59-74.
3. Paterson DL, (2006) Resistance in gram-negative bacteria: Enterobacteriaceae. American Journal of Infection Control 34: S20-S28.
4. Hammerum AM, Heuer OE, (2009) Human health hazards from antimicrobial-resistant Escherichia coli of animal origin. Clini Infect Dis 48: 916-921.
5. Johnson TJ, Skyberg J, Nolan LK, (2004) Multiple antimicrobial resistance region of a putative virulence plasmid from an Escherichia coli isolate incriminated in avian colibacillosis. Avian Dis 48: 351-360.
6. Fricke WF, McDermott PF, Mammel MK, Zhao SH, Johnson TJ, et al. (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 Environmen Microbiol 75: 5963-5971.
7. Johnson TJ, Jordan D, Kariyawasam S, Stell AL, Bell NP, et al. (2010) Sequence analysis and characterization of a transferable hybrid plasmid encoding multidrug resistance and enabling zoonotic potential for extraintestinal Escherichia coli. Infect Immun 78: 1931-1942.
8. Lindsey RL, Fedorka-Cray PJ, Frye JG, Meinersmann RJ, (2009) IncA/C plasmids are prevalent in multidrug-resistant Salmonella enterica isolates. Appl Environ Microbiol 75: 1908-1915.
9. Johnson TJ, Nolan LK, (2009) Plasmid replicon typing. Methods Mol Biol 551: 27-35.
10. Frost LS, Leplae R, Summers AO, Toussaint A, (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3: 722-732.
11. Shintani M, Takahashi Y, Tokumaru H, Kadota K, Hara H, et al. (2010) Response of the Pseudomonas host chromosomal transcriptome to carriage of the IncP-7 plasmid pCAR1. Environmen Microbiol 12: 1413-1426.
12. DebRoy C, Sidhu MS, Sarker U, Jayarao BM, Stell AL, et al. (2010) Complete sequence of pEC14_114, a highly conserved IncFIB/FIIA plasmid associated with uropathogenic Escherichia coli cystitis strains. Plasmid 63: 53-60.
13. Aoki T, Egusa S, Ogata Y, Watanabe T, (1971) Detection of resistance factors in fish pathogen Aeromonas liquefaciens. J Gen Microbiol 65: 343-349.
14. Fricke WF, Welch TJ, McDermott PF, Mammel MK, LeClerc JE, et al. (2009) Comparative genomics of the IncA/C multidrug resistance plasmid family. J Bacteriol 191: 4750-4757.
15. Galimand M, Guiyoule A, Gerbaud G, Rasoamanana B, Chanteau S, et al. (1997) Multidrug resistance in Yersinia pestis mediated by a transferrable plasmid. N Engl J Med 337: 677-680.
16. Welch TJ, Fricke WF, McDermott PF, White DG, Rosso ML, et al. (2007) Multiple antimicrobial resistance in plague: an emerging public health risk. PLoS One 2: e309.
17. Kim E, Aoki T, (1996) Sequence analysis of the florfenicol resistance gene encoded in the transferable R-plasmid of a fish pathogen, Pasteurella piscicida. Microbiol Immunol 40: 665-669.
18. Kim MJ, Hirono I, Kurokawa K, Maki T, Hawke J, et al. (2008) Complete DNA sequence and analysis of the transferable multiple-drug resistance plasmids (R Plasmids) from Photobacterium damselae subsp. piscicida isolates collected in Japan and the United States. Antimicrob Agents Chemother 52: 606-611.
19. Cloeckaert A, Baucheron S, Chaslus-Dancla E, (2001) Nonenzymatic chloramphenicol resistance mediated by IncC plasmid R55 is encoded by a floR gene variant. Antimicrob Agents Chemother 45: 2381-2382.
20. Hochhut B, Lotfi Y, Mazel D, Faruque SM, Woodgate R, et al. (2001) Molecular analysis of antibiotic resistance gene clusters in Vibrio cholerae O139 and O1SXT constins. Antimicrob Agents Chemother 45: 2991-3000.
21. Pan JC, Ye R, Wang HQ, Xiang HQ, Zhang W, et al. (2008) Vibrio cholerae O139 multiple-drug resistance mediated by Yersinia pestis pIP1202-like conjugative plasmids. Antimicrob Agents Chemother 52: 3829-3836.
22. Call DR, Singer RS, Meng D, Broschat SL, Orfe LH, et al. (2010) blaCMY-2-positive IncA/C plasmids from Escherichia coli and Salmonella enterica are a distinct component of a larger lineage of plasmids. Antimicrob Agents Chemother 54: 590-596.
23. Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, et al. (2010) Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis 10: 597-602.
24. Toleman MA, Bennett PM, Walsh TR, (2006) ISCR elements: novel gene-capturing systems of the 21st century? Microbiol Mol Biol Rev 70: 296-316.
25. Liebert CA, Hall RM, Summers AO, (1999) Transposon Tn21, flagship of the floating genome. Microbiol Mol Biol Rev 63: 507-522.
26. Yun CS, Suzuki C, Naito K, Takeda T, Takahashi Y, et al. (2010) Pmr, a histone-like protein H1 (H-NS) family protein encoded by the IncP-7 plasmid pCAR1, is a key global regulator that alters host function. J Bacteriol 192: 4720-4731.
27. Dillon SC, Cameron AD, Hokamp K, Lucchini S, Hinton JC, et al. (2010) Genome-wide analysis of the H-NS and Sfh regulatory networks in Salmonella Typhimurium identifies a plasmid-encoded transcription silencing mechanism. Mol Microbiol 76: 1250-1265.
28. Welch TJ, Evenhuis J, White DG, McDermott PF, Harbottle H, et al. (2009) IncA/C plasmid-mediated florfenicol resistance in the catfish pathogen Edwardsiella ictaluri. Antimicrob Agents Chemother 53: 845-846.
29. Singh A, Zhao S, Sabo JL, Abbott JW, Fields PI, et al. (2011) Plasmid replicon typing of historical Salmonella Newport: 1940-2000; New Orleans, LA.
30. Tadesse DA, Zhao S, Harbottle H, Mcdermott PF, (2011) Plasmid diversity among historical E. coli isolates of human and animal origin, 1950s-2000s; New Orleans, LA.
31. Wiesner M, Calva E, Fernandez-Mora M, Cevallos MA, Campos F, et al. (2011) Salmonella Typhimurium ST213 is associated with two types of IncA/C plasmids carrying multiple resistance determinants. BMC Microbiol 11: 9.
32. Glenn LM, Lindsey RL, Frank JF, Meinersmann RJ, Englen MD, et al. (2011) Analysis of antimicrobial resistance genes detected in multidrug-resistant Salmonella enterica serovar Typhimurium isolated from food animals. Microb Drug Resist., Epub Ahead of Print.
33. Lindsey RL, Frye JG, Thitaram SN, Meinersmann RJ, Fedorka-Cray PJ, et al. (2011) Characterization of multidrug-resistant Escherichia coli by antimicrobial resistance profiles, plasmid replicon typing, and pulsed-field gel electrophoresis. Microb Drug Resist 17: 157-163.
34. Lindsey RL, Fedorka-Cray PJ, Frye JG, Meinersmann RJ, (2009) IncA/C plasmids are prevalent in multidrug-resistant Salmonella enterica isolates. Appl Environ Microbiol 75: 1908-1915.
35. Alcaine SD, Sukhnanand SS, Warnick LD, Su WL, McGann P, et al. (2005) Ceftiofur-resistant Salmonella strains isolated from dairy farms represent multiple widely distributed subtypes that evolved by independent horizontal gene transfer. Antimicrobial Agents and Chemotherapy 49: 4061-4067.
36. Brinas L, Moreno MA, Zarazaga M, Porrero C, Saenz Y, et al. (2003) Detection of CMY-2, CTX-M-14, and SHV-12 beta-lactamases in Escherichia coli fecal-sample isolates from healthy chickens. Antimicrob Agents Chemother 47: 2056-2058.
37. Carattoli A, Tosini F, Giles WP, Rupp ME, Hinrichs SH, et al. (2002) Characterization of plasmids carrying CMY-2 from expanded-spectrum cephalosporin-resistant Salmonella strains isolated in the United States between 1996 and 1998. Antimicrob Agents Chemother 46: 1269-1272.
38. Dierikx C, van Essen-Zandbergen A, Veldman K, Smith H, Mevius D, (2010) Increased detection of extended spectrum beta-lactamase producing Salmonella enterica and Escherichia coli isolates from poultry. Vet Microbiol 145: 273-278.
39. Doublet B, Carattoli A, Whichard JM, White DG, Baucheron S, et al. (2004) Plasmid-mediated florfenicol and ceftriaxone resistance encoded by the floR and bla(CMY-2) genes in Salmonella enterica serovars Typhimurium and Newport isolated in the United States. FEMS Microbiol Lett 233: 301-305.
40. Frye JG, Fedorka-Cray PJ, (2007) Prevalence, distribution and characterisation of ceftiofur resistance in Salmonella enterica isolated from animals in the USA from 1999 to 2003. Int J Antimicrob Agents 30: 134-142.
41. Gonzalez-Sanz R, Herrera-Leon S, de la Fuente M, Arroyo M, Echeita MA, (2009) Emergence of extended-spectrum beta-lactamases and AmpC-type beta-lactamases in human Salmonella isolated in Spain from 2001 to 2005. J Antimicrob Chemother 64: 1181-1186.
42. Zaidi MB, Leon V, Canche C, Perez C, Zhao S, et al. (2007) Rapid and widespread dissemination of multidrug-resistant blaCMY-2 Salmonella Typhimurium in Mexico. J Antimicrob Chemother 60: 398-401.
43. Toleman MA, Walsh TR, (2011) Combinatorial events of insertion sequences and ICE in Gram-negative bacteria. FEMS Microbiol Rev., Epub Ahead of Print.
44. D'Andrea MM, Literacka E, Zioga A, Giani T, Baraniak A, et al. (2011) Evolution and spread of a multidrug-resistant Proteus mirabilis clone with chromosomal AmpC-type cephalosporinases in Europe. Antimicrob Agents Chemother 55: 2735-2742.
45. Toleman MA, Walsh TR, (2008) Evolution of the ISCR3 group of ISCR elements. Antimicrob Agents Chemother 52: 3789-3791.
46. Toleman MA, Walsh TR, (2010) ISCR elements are key players in IncA/C plasmid evolution. Antimicrob Agents Chemother 54: 3534; author reply 3534.
47. Suzuki H, Yano H, Brown CJ, Top EM, (2010) Predicting plasmid promiscuity based on genomic signature. J Bacteriol 192: 6045-6055.
48. Dorman CJ, (2009) Nucleoid-associated proteins and bacterial physiology. Adv Appl Microbiol 67: 47-64.
49. Doyle M, Fookes M, Ivens A, Mangan MW, Wain J, et al. (2007) An H-NS-like stealth protein aids horizontal DNA transmission in bacteria. Science 315: 251-252.
50. Noguchi N, Takada K, Katayama J, Emura A, Sasatsu M, (2000) Regulation of transcription of the mph(A) gene for macrolide 2′-phosphotransferase I in Escherichia coli: characterization of the regulatory gene mphR(A). J Bacteriol 182: 5052-5058.
51. Gonzalez-Zorn B, Teshager T, Casas M, Porrero MC, Moreno MA, et al. (2005) armA and aminoglycoside resistance in Escherichia coli. Emerg Infect Dis 11: 954-956.
52. Golebiewski M, Kern-Zdanowicz I, Zienkiewicz M, Adamczyk M, Zylinska J, et al. (2007) Complete nucleotide sequence of the pCTX-M3 plasmid and its involvement in spread of the extended-spectrum beta-lactamase gene blaCTX-M-3. Antimicrob Agents Chemother 51: 3789-3795.
53. Singer RS, Patterson SK, Wallace RL, (2008) Effects of therapeutic ceftiofur administration to dairy cattle on Escherichia coli dynamics in the intestinal tract. Appl Environ Microbiol 74: 6956-6962.
54. Folster JP, Pecic G, Bolcen S, Theobald L, Hise K, et al. (2010) Characterization of extended-spectrum cephalosporin-resistant Salmonella enterica serovar Heidelberg isolated from humans in the United States. Foodborne Pathog Dis 7: 181-187.
55. Zhao S, White DG, Friedman SL, Glenn A, Blickenstaff K, et al. (2008) Antimicrobial resistance in Salmonella enterica serovar Heidelberg isolates from retail meats, including poultry, from 2002 to 2006. Appl Environ Microbiol 74: 6656-6662.
56. Subbiah M, Top EM, Shah DH, Call DR, (2011) Selection pressure required for long-term persistence of blaCMY-2-positive IncA/C plasmids. Appl Environ Microbiol 77: 4486-4493.
57. Bradley DE, (1989) Conjugation system of IncC plasmid RA1, and the interaction of RA1 pili with specific RNA phage C-1. Res Microbiol 140: 439-446.
58. Poirel L, Schrenzel J, Cherkaoui A, Bernabeu S, Renzi G, et al. (2011) Molecular analysis of NDM-1-producing enterobacterial isolates from Geneva, Switzerland. J Antimicrob Chemother.
59. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
60. Zhang Z, Schwartz S, Wagner L, Miller W, (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7: 203-214.
61. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
62. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular biology and evolution 24: 1596-1599.