Insertion sequence IS26 reorganizes plasmids in clinically isolated multidrug-resistant bacteria by replicative transposition

mBio

Volumn 6, Issue 3, 2015, Pages

  He, Susu ^a   Hickman, Alison Burgess ^a   Varani, Alessandro M ^b   Siguier, Patricia ^c   Chandler, Michael ^c   Dekker, John P ^d   Dyda, Fred ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c CNRS   (France)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; CARBAPENEMASE; BACTERIAL PROTEIN; BETA LACTAMASE; TRANSPOSON;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; BLAKPC GENE; CARBAPENEMASE PRODUCING ENTEROBACTERIACEAE; CITROBACTER FREUNDII; CONTROLLED STUDY; DNA FLANKING REGION; DNA TRANSPOSITION; ENTEROBACTER CLOACAE; ESCHERICHIA COLI; GENE CLUSTER; GENE DELETION; GENE DOSAGE; GENE DUPLICATION; GENE FUSION; GENE INSERTION SEQUENCE; GENE REARRANGEMENT; GENETIC DATABASE; GENOME ANALYSIS; GENOMICS; GENOTYPE PHENOTYPE CORRELATION; HETEROZYGOTE; KLEBSIELLA OXYTOCA; KLEBSIELLA PNEUMONIAE; MULTIDRUG RESISTANCE; NONHUMAN; PANTOEA; PLASMID; PRIORITY JOURNAL; REPLICON; SEQUENCE HOMOLOGY; STRAIN DIFFERENCE; TRANSPOSON; DNA REPLICATION; DRUG EFFECTS; ENTEROBACTERIACEAE; ENTEROBACTERIACEAE INFECTION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; NATIONAL HEALTH ORGANIZATION; UNITED STATES;

ENTEROBACTERIACEAE;

BACTERIAL PROTEINS; BETA-LACTAMASES; DNA REPLICATION; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENTEROBACTERIACEAE; ENTEROBACTERIACEAE INFECTIONS; GENE REARRANGEMENT; HUMANS; MUTAGENESIS, INSERTIONAL; NATIONAL INSTITUTES OF HEALTH (U.S.); PLASMIDS; UNITED STATES;

EID: 84936970574     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00762-15     Document Type: Article

References (66)

1. McKenna M. 2013. Antibiotic resistance: the last resort. Nature 499: 394-396. http://dx.doi.org/10.1038/499394a.
2. Hedges RW, Jacob AE. 1974. Transposition of ampicillin resistance from RP4 to other replicons. Mol Gen Genet 132:31-40. http://dx.doi.org/ 10.1007/BF00268228.
3. Kiiru J, Butaye P, Goddeeris BM, Kariuki S. 2013. Analysis for prevalence and physical linkages amongst integrons, ISEcp1, ISCR1, Tn21 and Tn7 encountered in Escherichia coli strains from hospitalized and nonhospitalized patients in Kenya during a 19-year period (1992-2011).BMC Microbiol 13:109. http://dx.doi.org/10.1186/1471-2180-13-109.
4. Dhanji H, Doumith M, Hope R, Livermore DM, Woodford N. 2011. ISEcp1-mediated transposition of linked blaCTX-M-3 and blaTEM-1b from the IncI1 plasmid pEK204 found in clinical isolates of Escherichia coli from Belfast, UK. J Antimicrob Chemother 66:2263-2265. http://dx.doi.org/ 10.1093/jac/dkr310.
5. Wang Y, Song C, Duan G, Zhu J, Yang H, Xi Y, Fan Q. 2013. Transposition of ISEcp1 modulates blaCTX-M-55-mediated Shigella flexneri resistance to cefalothin. Int J Antimicrob Agents 42:507-512. http:// dx.doi.org/10.1016/j.ijantimicag.2013.08.009.
6. Karim A, Poirel L, Nagarajan S, Nordmann P. 2001. Plasmid-mediated extended-spectrum beta-lactamase (CTX-M-3 like) from India and gene association with insertion sequence ISEcp1. FEMS Microbiol Lett 201: 237-241. http://dx.doi.org/10.1016/S0378-1097(01)00276-2.
7. Naas T, Cuzon G, Villegas MV, Lartigue MF, Quinn JP, Nordmann P. 2008. Genetic structures at the origin of acquisition of the beta-lactamase blaKPC gene. Antimicrob Agents Chemother 52:1257-1263. http:// dx.doi.org/10.1128/AAC.01451-07.
8. Gootz TD, Lescoe MK, Dib-Hajj F, Dougherty BA, He W, Della-Latta P, Huard RC. 2009. Genetic organization of transposase regions surrounding blaKPC carbapenemase genes on plasmids from Klebsiella strains isolated in a New York City hospital. Antimicrob Agents Chemother 53: 1998-2004. http://dx.doi.org/10.1128/AAC.01355-08.
9. Partridge SR, Iredell JR. 2012. Genetic contexts of blaNDM-1. Antimicrob Agents Chemother 56:6065-6067. http://dx.doi.org/10.1128/AAC.00117-12.
10. Pfeifer Y, Wilharm G, Zander E, Wichelhaus TA, Göttig S, Hunfeld KP, Seifert H, Witte W, Higgins PG. 2011. Molecular characterization of blaNDM-1 in an Acinetobacter baumannii strain isolated in Germany in 2007. J Antimicrob Chemother 66:1998-2001. http://dx.doi.org/10.1093/ jac/dkr256.
11. Mazel D. 2006. Integrons: agents of bacterial evolution. Nat Rev Microbiol 4:608-620. http://dx.doi.org/10.1038/nrmicro1462.
12. Stokes HW, Hall RM. 1989. A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: integrons. Mol Microbiol 3:1669-1683. http://dx.doi.org/10.1111/j.1365-2958.1989.tb00153.x.
13. Roy Chowdhury P, Ingold A, Vanegas N, Martínez E, Merlino J, Merkier AK, Castro M, González Rocha G, Borthagaray G, Centrón D, Bello Toledo H, Márquez CM, StokesHW. 2011. Dissemination of multiple drug resistance genes by class 1 integrons in Klebsiella pneumoniae isolates from four countries: a comparative study. Antimicrob Agents Chemother 55: 3140-3149. http://dx.doi.org/10.1128/AAC.01529-10.
14. Partridge SR, Recchia GD, Scaramuzzi C, Collis CM, Stokes HW, Hall RM. 2000. Definition of the attI1 site of class 1 integrons. Microbiology 146:2855-2864.
15. Toleman MA, Bennett PM, Walsh TR. 2006. ISCR elements: novel genecapturing systems of the 21st century? Microbiol Mol Biol Rev 70: 296-316. http://dx.doi.org/10.1128/MMBR.00048-05.
16. Siguier P, Gourbeyre E, ChandlerM. 2014. Bacterial insertion sequences: their genomic impact and diversity. FEMS Microbiol Rev 38:865-891. http://dx.doi.org/10.1111/1574-6976.12067.
17. Olliver A, Vallé M, Chaslus-Dancla E, Cloeckaert A. 2005. Overexpression of the multidrug efflux operon acrEF by insertional activation with IS1 or IS10 elements in Salmonella enterica serovar Typhimurium DT204 acrB mutants selected with fluoroquinolones. Antimicrob Agents Chemother 49:289-301. http://dx.doi.org/10.1128/AAC.49.1.289-301.2005.
18. Jellen-Ritter AS, Kern WV. 2001. Enhanced expression of the multidrug efflux pumps AcrAB and AcrEF associated with insertion element transposition in Escherichia coli mutants selected with a fluoroquinolone. Antimicrob Agents Chemother 45:1467-1472. http://dx.doi.org/10.1128/ AAC.45.5.1467-1472.2001.
19. Toleman MA, Walsh TR. 2011. Combinatorial events of insertion sequences and ICE in gram-negative bacteria. FEMS Microbiol Rev 35: 912-935. http://dx.doi.org/10.1111/j.1574-6976.2011.00294.x.
20. Schubert S, Dufke S, Sorsa J, Heesemann J. 2004. A novel integrative and conjugative element (ICE) of Escherichia coli: the putative progenitor of the Yersinia high-pathogenicity island. Mol Microbiol 51:837-848. http:// dx.doi.org/10.1046/j.1365-2958.2003.03870.x.
21. Mahillon J, Chandler M. 1998. Insertion sequences. Microbiol Mol Biol Rev 62:725-774.
22. Siguier P, Filée J, Chandler M. 2006. Insertion sequences in prokaryotic genomes. Curr Opin Microbiol 9:526-531. http://dx.doi.org/10.1016/ j.mib.2006.08.005.
23. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. 2006. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34:D32-D36. http://dx.doi.org/10.1093/nar/gkj014.
24. Dyda F, Hickman AB, Jenkins TM, Engelman A, Craigie R, Davies DR. 1994. Crystal structure of the catalytic domain of HIV-1 integrase: similarity to other polynucleotidyl transferases. Science 266:1981-1986. http:// dx.doi.org/10.1126/science.7801124.
25. Hickman AB, Chandler M, Dyda F. 2010. Integrating prokaryotes and eukaryotes: DNA transposases in light of structure. Crit Rev Biochem Mol Biol 45:50-69. http://dx.doi.org/10.3109/10409230903505596.
26. Curcio MJ, DerbyshireKM. 2003. The outs and ins of transposition: from Mu to kangaroo. Nat Rev Mol Cell Biol 4:865-877. http://dx.doi.org/ 10.1038/nrm1241.
27. Arthur A, Sherratt D. 1979. Dissection of the transposition process: a transposon-encoded site-specific recombination system. Mol Gen Genet 175:267-274. http://dx.doi.org/10.1007/BF00397226.
28. Shapiro JA. 1979. Molecular model for the transposition and replication of bacteriophage Mu and other transposable elements. Proc Natl Acad Sci U S A 76:1933-1937. http://dx.doi.org/10.1073/pnas.76.4.1933.
29. Snitkin ES, Zelazny AM, Thomas PJ, Stock F, NISC Comparative Sequencing Program Group, Henderson DK, Palmore TN, Segre JA. 2012. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med 4:148ra116. http://dx.doi.org/10.1126/scitranslmed.3004129.
30. Conlan S, Thomas PJ, Deming C, Park M, Lau AF, Dekker JP, Snitkin ES, Clark TA, Luong K, Song Y, Tsai YC, Boitano M, Dayal J, Brooks SY, Schmidt B, Young AC, Thomas JW, Bouffard GG, Blakesley RW, NISC Comparative Sequencing Program, Mullikin JC, Korlach J, Henderson DK, Frank KM, Palmore TN, Segre JA. 2014. Single-molecule sequencing to track plasmid diversity of hospital-associated carbapenemase-producing Enterobacteriaceae. Sci Transl Med 6:254ra126. http://dx.doi.org/10.1126/scitranslmed.3009845.
31. Chen L, Chavda KD, Melano RG, Jacobs MR, Koll B, Hong T, Rojtman AD, Levi MH, Bonomo RA, Kreiswirth BN. 2014. Comparative genomic analysis of KPC-encoding pKpQIL-like plasmids and their distribution in New Jersey and New York hospitals. Antimicrob Agents Chemother 58: 2871-2877. http://dx.doi.org/10.1128/AAC.00120-14.
32. Leavitt A, Chmelnitsky I, Carmeli Y, Navon-Venezia S. 2010. Complete nucleotide sequence of KPC-3-encoding plasmid pKpQIL in the epidemic Klebsiella pneumoniae sequence type 258. Antimicrob Agents Chemother 54:4493-4496. http://dx.doi.org/10.1128/AAC.00175-10.
33. Varani AM, Siguier P, Gourbeyre E, Charneau V, Chandler M. 2011. ISsaga is an ensemble of web-based methods for high throughput identification and semi-automatic annotation of insertion sequences in prokaryotic genomes. Genome Biol 12:R30. http://dx.doi.org/10.1186/gb-2011-12-3-r30.
34. Dyda F, Chandler M, Hickman AB. 2012. The emerging diversity of transpososome architectures. Q Rev Biophys 45:493-521. http:// dx.doi.org/10.1017/S0033583512000145.
35. Hudson CM, Bent ZW, Meagher RJ, Williams KP. 2014. Resistance determinants and mobile genetic elements of an NDM-1-encoding Klebsiella pneumoniae strain. PLoS ONE 9:e99209. http://dx.doi.org/10.1371/ journal.pone.0099209.
36. Mollet B, Iida S, Shepherd J, Arber W. 1983. Nucleotide sequence of IS26, a new prokaryotic mobile genetic element. Nucleic Acids Res 11: 6319-6330. http://dx.doi.org/10.1093/nar/11.18.6319.
37. Iida S, Meyer J, Linder P, Goto N, Nakaya R, Reif HJ, Arber W. 1982. The kanamycin resistance transposon Tn2680 derived from the R plasmid Rts1 and carried by phage P1Km has flanking 0.8-kb-long direct repeats. Plasmid 8:187-198. http://dx.doi.org/10.1016/0147-619X(82)90056-7.
38. Iida S, Mollet B, Meyer J, Arber W. 1984. Functional characterization of the prokaryotic mobile genetic element IS26. Mol Gen Genet 198:84-89. http://dx.doi.org/10.1007/BF00328705.
39. Trieu-Cuot P, Courvalin P. 1985. Transposition behavior of IS15 and its progenitor IS15-Δ: are cointegrates exclusive end products? Plasmid 14: 80-89. http://dx.doi.org/10.1016/0147-619X(85)90034-4.
40. Villa L, García-Fernández A, Fortini D, Carattoli A. 2010. Replicon sequence typing of IncF plasmids carrying virulence and resistance determinants. J Antimicrob Chemother 65:2518-2529. http://dx.doi.org/ 10.1093/jac/dkq347.
41. DeLeo FR, Chen L, Porcella SF, Martens CA, Kobayashi SD, Porter AR, Chavda KD, Jacobs MR, Mathema B, Olsen RJ, Bonomo RA, Musser JM, Kreiswirth BN. 2014. Molecular dissection of the evolution of carbapenem-resistant multilocus sequence type 258 Klebsiella pneumoniae. Proc Natl Acad Sci U S A 111:4988-4993. http://dx.doi.org/ 10.1073/pnas.1321364111.
42. Tolmasky ME, Crosa JH. 1987. Tn1331, a novel multiresistance transposon encoding resistance to amikacin and ampicillin in Klebsiella pneumoniae. Antimicrob Agents Chemother 31:1955-1960. http://dx.doi.org/ 10.1128/AAC.31.12.1955.
43. Tolmasky ME, Crosa JH. 1993. Genetic organization of antibiotic resistance genes (aac(6=)-Ib, aadA, and oxa9) in the multiresistance transposon Tn1331. Plasmid 29:31-40. http://dx.doi.org/10.1006/plas.1993.1004.
44. Chen L, Chavda KD, Al Laham N, Melano RG, Jacobs MR, Bonomo RA, Kreiswirth BN. 2013. Complete nucleotide sequence of a blaKPCharboring IncI2 plasmid and its dissemination in New Jersey and New York hospitals. Antimicrob Agents Chemother 57:5019-5025. http:// dx.doi.org/10.1128/AAC.01397-13.
45. Chandler M, Galas DJ. 1983. IS1-mediated tandem duplication of plasmid pBR322. Dependence on recA and on DNA polymerase I. J Mol Biol 165:183-190. http://dx.doi.org/10.1016/S0022-2836(83)80249-6.
46. Smith GP. 1976. Evolution of repeated DNA sequences by unequal crossover. Science 191:528-535. http://dx.doi.org/10.1126/science.1251186.
47. Billard-Pomares T, Fouteau S, Jacquet ME, Roche D, Barbe V, Castellanos M, Bouet JY, Cruveiller S, Médigue C, Blanco J, Clermont O, Denamur E, Branger C. 2014. Characterization of a P1-like bacteriophage carrying an SHV-2 extended-spectrum beta-lactamase from an Escherichia coli strain. Antimicrob Agents Chemother 58:6550-6557. http:// dx.doi.org/10.1128/AAC.03183-14.
48. Turlan C, Chandler M. 1995. IS1-mediated intramolecular rearrangements: formation of excised transposon circles and replicative deletions. EMBO J 14:5410-5421.
49. Naas T, Cuzon G, Truong HV, Nordmann P. 2012. Role of ISKpn7 and deletions in blaKPC gene expression. Antimicrob Agents Chemother 56: 4753-4759. http://dx.doi.org/10.1128/AAC.00334-12.
50. Lambin M, Nicolas E, Oger CA, Nguyen N, Prozzi D, Hallet B. 2012. Separate structural and functional domains of Tn4430 transposase contribute to target immunity. Mol Microbiol 83:805-820. http://dx.doi.org/ 10.1111/j.1365-2958.2012.07967.x.
51. Cuzon G, Naas T, Nordmann P. 2011. Functional characterization of Tn4401, a Tn3-based transposon involved in blaKPC gene mobilization. Antimicrob Agents Chemother 55:5370-5373. http://dx.doi.org/10.1128/ AAC.05202-11.
52. Bertini A, Poirel L, Bernabeu S, Fortini D, Villa L, Nordmann P, Carattoli A. 2007. Multicopy blaOXA-58 gene as a source of high-level resistance to carbapenems in Acinetobacter baumannii. Antimicrob Agents Chemother 51: 2324-2328. http://dx.doi.org/10.1128/AAC.01502-06.
53. Lee SY, Park YJ, Yu JK, Jung S, Kim Y, Jeong SH, Arakawa Y. 2012. Prevalence of acquired fosfomycin resistance among extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae clinical isolates in Korea and IS26-composite transposon surrounding fosA3. J Antimicrob Chemother 67:2843-2847. http://dx.doi.org/10.1093/jac/ dks319.
54. Miriagou V, Carattoli A, Tzelepi E, Villa L, Tzouvelekis LS. 2005. IS26-associated In4-type integrons forming multiresistance loci in enterobacterial plasmids. Antimicrob Agents Chemother 49:3541-3543. http:// dx.doi.org/10.1128/AAC.49.8.3541-3543.2005.
55. Harmer CJ, Moran RA, Hall RM. 2014. 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 5(5): e01801-01814. http://dx.doi.org/10.1128/mBio.01801-14.
56. Dutra BE, Sutera VA, Jr, Lovett ST. 2007. RecA-independent recombination is efficient but limited by exonucleases. Proc Natl Acad Sci U S A 104:216-221. http://dx.doi.org/10.1073/pnas.0608293104.
57. Loot C, Turlan C, Chandler M. 2004. Host processing of branched DNA intermediates is involved in targeted transposition of IS911. Mol Microbiol 51:385-393. http://dx.doi.org/10.1046/j.1365-2958.2003.03850.x.
58. Loot C, Turlan C, Rousseau P, Ton-Hoang B, Chandler M. 2002. A target specificity switch in IS911 transposition: the role of the OrfA protein. EMBO J 21:4172-4182. http://dx.doi.org/10.1093/emboj/cdf403.
59. Olasz F, Stalder R, Arber W. 1993. Formation of the tandem repeat (IS30)2 and its role in IS30-mediated transpositional DNA rearrangements. Mol Gen Genet 239:177-187.
60. Turlan C, Loot C, Chandler M. 2004. IS911 partial transposition products and their processing by the Escherichia coli RecG helicase. Mol Microbiol 53:1021-1033. http://dx.doi.org/10.1111/j.1365-2958.2004.04165.x.
61. Parkhill J, Sebaihia M, Preston A, Murphy LD, Thomson N, Harris DE, Holden MTG, Churcher CM, Bentley SD, Mungall KL, Cerdeño-Tárraga AM, Temple L, James K, Harris B, Quail MA, Achtman M, Atkin R, Baker S, Basham D, Bason N, Cherevach I, Chillingworth T, Collins M, Cronin A, Davis P, Doggett J, Feltwell T, Goble A, Hamlin N, Hauser H, Holroyd S, Jagels K, Leather S, Moule S, Norberczak H, O'Neil S, Ormond D, Price C, Rabbinowitsch E, Rutter S, Sanders M, Saunders D, Seeger K, Sharp S, Simmonds M, Skelton J, Squares R, Squares S, Stevens K, Unwin L, Whitehead S, Barrell BG, Maskell DJ. 2003. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35: 32-40. http://dx.doi.org/10.1038/ng1227.
62. Lesic B, Zouine M, Ducos-Galand M, Huon C, Rosso ML, Prévost MC, Mazel D, Carniel E. 2012. A natural system of chromosome transfer in Yersinia pseudotuberculosis. PLoS Genet 8:e1002529. http://dx.doi.org/ 10.1371/journal.pgen.1002529.
63. Weinert TA, Schaus NA, Grindley ND. 1983. Insertion sequence duplication in transpositional recombination. Science 222:755-765. http:// dx.doi.org/10.1126/science.6314502.
64. Blake DG, Boocock MR, Sherratt DJ, Stark WM. 1995. Cooperative binding of Tn3 resolvase monomers to a functionally asymmetric binding site. Curr Biol 5:1036-1046. http://dx.doi.org/10.1016/S0960-9822 (95)00208-9.
65. Galas DJ, Chandler M. 1982. Structure and stability of Tn9-mediated cointegrates. Evidence for two pathways of transposition. J Mol Biol 154: 245-272. http://dx.doi.org/10.1016/0022-2836(82)90063-8.
66. Grindley NDF, Joyce CM. 1981. Analysis of the structure and function of the kanamycin-resistance transposon Tn903. Cold Spring Harb Symp Quant Biol 45:125-133. http://dx.doi.org/10.1101/SQB.1981.045.01.021.