Tn6026 and Tn6029 are found in complex resistance regions mobilised by diverse plasmids and chromosomal islands in multiple antibiotic resistant Enterobacteriaceae

Plasmid

Volumn 80, Issue , 2015, Pages 127-137

  Reid, Cameron J ^a   Chowdhury, Piklu Roy ^a,b   Djordjevic, Steven P ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b NSW DEPARTMENT OF PRIMARY INDUSTRIES   (Australia)

Author keywords

Complex resistance loci; Composite transposon like; Composite transposons; IS26; Tn6026; Tn6029

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; BETA LACTAM ANTIBIOTIC; KANAMYCIN; NEOMYCIN; STREPTOMYCIN; SULFAMETHOXAZOLE; TETRACYCLINE; TRIMETHOPRIM; TRANSPOSON;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL VIRULENCE; COMMENSAL ESCHERICHIA COLI; ENTEROAGGREGATIVE HEMORRHAGIC ESCHERICHIA COLI; ENTEROBACTERIACEAE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI; GENE CLUSTER; GENE LOCATION; GENE STRUCTURE; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOMIC ISLAND; GEOGRAPHIC DISTRIBUTION; MULTIDRUG RESISTANCE; NONHUMAN; OXIDATIVE STRESS; PATHOGENIC ESCHERICHIA COLI; PLASMID; SALMONELLA ENTERICA SEROVAR PARATYPHI A; SALMONELLA ENTERICA SEROVAR TYPHI; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; TN6026 GENE; TN6029 GENE; TRANSPOSON; ANIMAL; GENETICS; HUMAN; VIRULENCE;

ANIMALIA; ENTEROBACTERIACEAE; ESCHERICHIA COLI; SALMONELLA ENTERICA;

ANIMALS; CHROMOSOMES, BACTERIAL; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENTEROBACTERIACEAE; GENES, BACTERIAL; HUMANS; PLASMIDS; VIRULENCE;

EID: 84938747383     PISSN: 0147619X     EISSN: 10959890     Source Type: Journal    
DOI: 10.1016/j.plasmid.2015.04.005     Document Type: Article

References (80)

1. Ahmed S.A., et al. Genomic comparison of Escherichia coli O104:H4 isolates from 2009 and 2011 reveals plasmid, and prophage heterogeneity, including shiga toxin encoding phage stx2. PLoS ONE 2012, 7(11):e48228.
2. Bailey J.K., et al. Distribution of the blaTEM gene and blaTEM-containing transposons in commensal Escherichia coli. J. Antimicrob. Chemother 2011, 66(4):745-751.
3. Baquero F., Tobes R. Bloody coli: a gene cocktail in Escherichia coli O104:H4. MBio 2013, 4(1). e00066-13.
4. Billard-Pomares T., et al. Characterization of a P1-like bacteriophage carrying an SHV-2 extended-spectrum beta-lactamase from an Escherichia coli strain. Antimicrob. Agents Chemother 2014, 58(11):6550-6557.
5. Brzuszkiewicz E., et al. Genome sequence analyses of two isolates from the recent Escherichia coli outbreak in Germany reveal the emergence of a new pathotype: Entero-Aggregative-Haemorrhagic Escherichia coli (EAHEC). Arch. Microbiol 2011, 193(12):883-891.
6. Buchholz U., et al. German outbreak of Escherichia coli O104:H4 associated with sprouts. N. Engl. J. Med 2011, 365(19):1763-1770.
7. Burland V., et al. The complete DNA sequence and analysis of the large virulence plasmid of Escherichia coli O157:H7. Nucleic Acids Res 1998, 26(18):4196-4204.
8. Cain A.K., Hall R.M. Evolution of a multiple antibiotic resistance region in IncHI1 plasmids: reshaping resistance regions in situ. J. Antimicrob. Chemother 2012, 67(12):2848-2853.
9. Cain A.K., Hall R.M. Evolution of IncHI2 plasmids via acquisition of transposons carrying antibiotic resistance determinants. J. Antimicrob. Chemother 2012, 67(5):1121-1127.
10. Cain A.K., et al. Transposons related to Tn1696 in IncHI2 plasmids in multiply antibiotic resistant Salmonella enterica serovar Typhimurium from Australian animals. Microb. Drug Resist 2010, 16(3):197-202.
11. Chiou C.S., et al. Chromosome-mediated multidrug resistance in Salmonella enterica serovar Typhi. Antimicrob. Agents Chemother 2014, 59:721-723.
12. Chouikha I., et al. A selC-associated genomic island of the extraintestinal avian pathogenic Escherichia coli strain BEN2908 is involved in carbohydrate uptake and virulence. J. Bacteriol 2006, 188(3):977-987.
13. Chu P.Y., Peng C.F. Genetic environments of the transferable plasmid-mediated blaCTX-M-3 gene in Serratia marcescens isolates. Jpn. J. Infect. Dis 2014, 67(1):58-61.
14. Cloeckaert A., et al. Dissemination of an extended-spectrum-beta-lactamase blaTEM-52 gene-carrying IncI1 plasmid in various Salmonella enterica serovars isolated from poultry and humans in Belgium and France between 2001 and 2005. Antimicrob. Agents Chemother 2007, 51(5):1872-1875.
15. Conlan S., et al. Single-molecule sequencing to track plasmid diversity of hospital-associated carbapenemase-producing Enterobacteriaceae. Sci. Transl. Med 2014, 6(254):254ra126.
16. Daly M., et al. Comparison of multidrug resistance gene regions between two geographically unrelated Salmonella serotypes. J. Antimicrob. Chemother 2005, 55(4):558-561.
17. Dawes F.E., et al. Distribution of class 1 integrons with IS26-mediated deletions in their 3'-conserved segments in Escherichia coli of human and animal origin. PLoS ONE 2010, 5(9):e12754.
18. Deng H., et al. Identification of the multi-resistance gene cfr in Escherichia coli isolates of animal origin. PLoS ONE 2014, 9(7):e102378.
19. Dionisi A.M., et al. Molecular characterization of multidrug-resistant strains of Salmonella enterica serotype Typhimurium and Monophasic variant (S. 4,[5],12:i:-) isolated from human infections in Italy. Foodborne Pathog. Dis 2009, 6(6):711-717.
20. Djordjevic S.P., et al. Virulence properties and serotypes of Shiga toxin-producing Escherichia coli from healthy Australian slaughter-age sheep. J. Clin. Microbiol 2001, 39(5):2017-2021.
21. Djordjevic S.P., Stokes H.W., Roy Chowdhury P. Mobile elements, zoonotic pathogens and commensal bacteria: conduits for the delivery of resistance genes into humans, production animals and soil microbiota. Front Microbiol 2013, 4:86.
22. Doi Y., et al. Whole-genome assembly of Klebsiella pneumoniae coproducing NDM-1 and OXA-232 carbapenemases using single-molecule, real-time sequencing. Antimicrob. Agents Chemother 2014, 58(10):5947-5953.
23. Dolejska M., et al. Complete sequences of IncHI1 plasmids carrying blaCTX-M-1 and qnrS1 in equine Escherichia coli provide new insights into plasmid evolution. J. Antimicrob. Chemother 2014, 69(9):2388-2393.
24. Du X.X., et al. Genetic characteristics of blaNDM-1-positive plasmid in Citrobacter freundii isolate separated from a clinical infectious patient. J. Med. Microbiol 2013, 62(Pt 9):1332-1337.
25. Fabrega A., Vila J. Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin. Microbiol. Rev 2013, 26(2):308-341.
26. Golebiewski M., et al. 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 2007, 51(11):3789-3795.
27. Goussard S., Courvalin P. Sequence of the genes blaT-1B and blaT-2. Gene 1991, 102(1):71-73.
28. Grad Y.H., et al. Comparative genomics of recent Shiga toxin-producing Escherichia coli O104:H4: short-term evolution of an emerging pathogen. MBio 2013, 4(1). e00452-12.
29. Guerry P., van Embden J., Falkow S. Molecular nature of two nonconjugative plasmids carrying drug resistance genes. J. Bacteriol 1974, 117(2):619-630.
30. Hamel M.J., et al. Does cotrimoxazole prophylaxis for the prevention of HIV-associated opportunistic infections select for resistant pathogens in Kenyan adults?. Am. J. Trop. Med. Hyg 2008, 79(3):320-330.
31. Harmer C.J., Moran R.A., Hall R.M. Movement of IS26-associated antibiotic resistance genes occurs via a translocatable unit that includes a single IS26 and preferentially inserts adjacent to another IS26. MBio 2014, 5(5):e1801-e1814.
32. He L., et al. Complete nucleotide sequence of pHN7A8, an F33:A-:B- type epidemic plasmid carrying blaCTX-M-65, fosA3 and rmtB from China. J. Antimicrob. Chemother 2013, 68(1):46-50.
33. Herrero-Fresno A., et al. Transposition and homologous recombination drive evolution of pUO-StVR2, a multidrug resistance derivative of pSLT, the virulence plasmid specific of Salmonella enterica serovar Typhimurium. Infect. Genet. Evol 2015, 29:99-102.
34. Hochhut B., et al. Molecular analysis of antibiotic resistance gene clusters in vibrio cholerae O139 and O1 SXT constins. Antimicrob. Agents Chemother 2001, 45(11):2991-3000.
35. Holt K.E., et al. Multidrug-resistant Salmonella enterica serovar paratyphi A harbors IncHI1 plasmids similar to those found in serovar typhi. J. Bacteriol 2007, 189(11):4257-4264.
36. Hornitzky M.A., et al. Virulence properties and serotypes of Shiga toxin-producing Escherichia coli from healthy Australian cattle. Appl. Environ. Microbiol 2002, 68(12):6439-6445.
37. Hornitzky M.A., et al. Bovine feces from animals with gastrointestinal infections are a source of serologically diverse atypical enteropathogenic Escherichia coli and Shiga toxin-producing E. coli strains that commonly possess intimin. Appl. Environ. Microbiol 2005, 71(7):3405-3412.
38. Hou J., et al. Detection of the plasmid-encoded fosfomycin resistance gene fosA3 in Escherichia coli of food-animal origin. J. Antimicrob. Chemother 2013, 68(4):766-770.
39. Hudson C.M., et al. Resistance determinants and mobile genetic elements of an NDM-1-encoding Klebsiella pneumoniae strain. PLoS ONE 2014, 9(6):e99209.
40. Iida S., et al. Functional characterization of the prokaryotic mobile genetic element IS26. Mol. Gen. Genet 1984, 198(1):84-89.
41. Jiang Y., et al. Dissemination of a clone carrying a fosA3-harbouring plasmid mediates high fosfomycin resistance rate of KPC-producing Klebsiella pneumoniae in China. Int. J. Antimicrob. Agents 2014, 45:66-70.
42. Kariuki S., et al. Characterization of multidrug-resistant typhoid outbreaks in Kenya. J. Clin. Microbiol 2004, 42(4):1477-1482.
43. Labar A.S., et al. Regional dissemination of a trimethoprim-resistance gene cassette via a successful transposable element. PLoS ONE 2012, 7(5):e38142.
44. Lester S.C., et al. The carriage of Escherichia coli resistant to antimicrobial agents by healthy children in Boston, in Caracas, Venezuela, and in Qin Pu, China. N. Engl. J. Med 1990, 323(5):285-289.
45. Leverstein-van Hall M.A., et al. Multidrug resistance among Enterobacteriaceae is strongly associated with the presence of integrons and is independent of species or isolate origin. J. Infect. Dis 2003, 187(2):251-259.
46. Lucarelli C., et al. Nucleotide sequence of the chromosomal region conferring multidrug resistance (R-type ASSuT) in Salmonella Typhimurium and monophasic Salmonella Typhimurium strains. J. Antimicrob. Chemother 2012, 67(1):111-114.
47. Mariani-Kurkdjian P., et al. Escherichia coli O104:H4 south-west France, June 2011. Lancet Infect. Dis 2011, 11(10):732-733.
48. Martinez E., et al. Establishment and multi drug resistance evolution of ST235 Pseudomonas aeruginosa strains in the intensive care unit of a Colombian hospital. Res. Microbiol 2014, 165(10):852-856.
49. Martinez J.L., Baquero F. Interactions among strategies associated with bacterial infection: pathogenicity, epidemicity, and antibiotic resistance. Clin. Microbiol. Rev 2002, 15(4):647-679.
50. Mollet B., et al. Nucleotide sequence of IS26, a new prokaryotic mobile genetic element. Nucleic Acids Res 1983, 11(18):6319-6330.
51. Mollet B., Iida S., Arber W. Gene organization and target specificity of the prokaryotic mobile genetic element IS26. Mol. Gen. Genet 1985, 201(2):198-203.
52. Nataro J.P., Kaper J.B. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev 1998, 11(1):142-201.
53. Nigro S.J., et al. A novel family of genomic resistance islands, AbGRI2, contributing to aminoglycoside resistance in Acinetobacter baumannii isolates belonging to global clone 2. J. Antimicrob. Chemother 2013, 68(3):554-557.
54. Ogura Y., et al. Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 2009, 106(42):17939-17944.
55. Okeke I.N., Fayinka S.T., Lamikanra A. Antibiotic resistance in Escherichia coli from Nigerian students, 1986 1998. Emerg. Infect. Dis 2000, 6(4):393-396.
56. Pansegrau W., et al. Complete nucleotide sequence of Birmingham IncP alpha plasmids. Compilation and comparative analysis. J. Mol. Biol 1994, 239(5):623-663.
57. Parkhill J., et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 2001, 413(6858):848-852.
58. Partridge S.R., Hall R.M. In34, a complex In5 family class 1 integron containing orf513 and dfrA10. Antimicrob. Agents Chemother 2003, 47(1):342-349.
59. Partridge S.R., Hall R.M. Evolution of transposons containing blaTEM genes. Antimicrob. Agents Chemother 2005, 49(3):1267-1268.
60. Post V., White P.A., Hall R.M. Evolution of AbaR-type genomic resistance islands in multiply antibiotic-resistant Acinetobacter baumannii. J. Antimicrob. Chemother 2010, 65(6):1162-1170.
61. Radstrom P., Swedberg G., Skold O. Genetic analyses of sulfonamide resistance and its dissemination in gram-negative bacteria illustrate new aspects of R plasmid evolution. Antimicrob. Agents Chemother 1991, 35(9):1840-1848.
62. Roy Chowdhury P., Charles I.G., Djordjevic S.P. A role for Tn6029 in the evolution of the complex antibiotic resistance gene loci in genomic island 3 in Enteroaggregative hemorrhagic Escherichia coli O104:H4. PLoS ONE 2015, 10(2):e0115781.
63. Schmidt H., et al. Identification and characterization of a novel genomic island integrated at selC in locus of enterocyte effacement-negative, Shiga toxin-producing Escherichia coli. Infect. Immun 2001, 69(11):6863-6873.
64. Shiga Y., Sekine Y., Ohtsubo E. Transposition of IS1 circles. Genes Cells 1999, 4(10):551-561.
65. Siebor E., Neuwirth C. Emergence of Salmonella genomic island 1 (SGI1) among Proteus mirabilis clinical isolates in Dijon, France. J. Antimicrob. Chemother 2013, 68(8):1750-1756.
66. Siebor E., Neuwirth C. Proteus genomic island 1 (PGI1), a new resistance genomic island from two Proteus mirabilis French clinical isolates. J. Antimicrob. Chemother 2014, 69(12):3216-3220.
67. Sun J., et al. Complete Nucleotide Sequence of cfr-Carrying IncX4 Plasmid pSD11 from Escherichia coli. Antimicrob. Agents Chemother 2015, 59(1):738-741.
68. Szczepanowski R., et al. The 120 592 bp IncF plasmid pRSB107 isolated from a sewage-treatment plant encodes nine different antibiotic-resistance determinants, two iron-acquisition systems and other putative virulence-associated functions. Microbiology 2005, 151(Pt 4):1095-1111.
69. Tamamura Y., et al. Complete nucleotide sequences of virulence-resistance plasmids carried by emerging multidrug-resistant Salmonella enterica Serovar Typhimurium isolated from cattle in Hokkaido, Japan. PLoS ONE 2013, 8(10):e77644.
70. Tran H.H., et al. Risk factors associated with typhoid fever in Son La province, northern Vietnam. Trans. R. Soc. Trop. Med. Hyg 2005, 99(11):819-826.
71. Uemura S., et al. Acquisition of a transposon encoding extended-spectrum beta-lactamase SHV-12 by Pseudomonas aeruginosa isolates during the clinical course of a burn patient. Antimicrob. Agents Chemother 2010, 54(9):3956-3959.
72. Venturini C., et al. Multiple antibiotic resistance gene recruitment onto the enterohemorrhagic Escherichia coli virulence plasmid. FASEB J. 2010, 24(4):1160-1166.
73. Venturini C., et al. Sequences of two related multiple antibiotic resistance virulence plasmids sharing a unique IS26-related molecular signature isolated from different Escherichia coli pathotypes from different hosts. PLoS ONE 2013, 8(11):e78862.
74. Vincent A.T., et al. Detection of Variants of the pRAS3, pAB5S9, and pSN254 Plasmids in Aeromonas salmonicida subsp. salmonicida: multidrug resistance, interspecies exchanges, and plasmid reshaping. Antimicrob. Agents Chemother 2014, 58(12):7367-7374.
75. Wain J., et al. Molecular analysis of incHI1 antimicrobial resistance plasmids from salmonella serovar typhi strains associated with typhoid fever. Antimicrob. Agents Chemother 2003, 47(9):2732-2739.
76. Wibberg D., et al. The IncF plasmid pRSB225 isolated from a municipal wastewater treatment plant's on-site preflooder combining antibiotic resistance and putative virulence functions is highly related to virulence plasmids identified in pathogenic E. coli isolates. Plasmid 2013, 69(2):127-137.
77. Williams L.E., et al. Facile recovery of individual high-molecular-weight, low-copy-number natural plasmids for genomic sequencing. Appl. Environ. Microbiol 2006, 72(7):4899-4906.
78. Wrighton C.J., Strike P. A pathway for the evolution of the plasmid NTP16 involving the novel kanamycin resistance transposon Tn4352. Plasmid 1987, 17(1):37-45.
79. Yau S., et al. RSF1010-like plasmids in Australian Salmonella enterica serovar Typhimurium and origin of their sul2-strA-strB antibiotic resistance gene cluster. Microb. Drug Resist 2010, 16(4):249-252.
80. Zhang W.J., et al. A novel conjugative plasmid from Escherichia coli of swine origin that co-harbors the multi-resistance gene cfr and the extended-spectrum beta-lactamase gene blaCTX-M-14b. Antimicrob. Agents Chemother 2014, 59:1337-1340.