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Mechanisms of Resistance

International Spread and Persistence of TEM-24 Is Caused by the Confluence of Highly Penetrating Enterobacteriaceae Clones and an IncA/C2 Plasmid Containing Tn1696::Tn1 and IS5075-Tn21

Ângela Novais, Fernando Baquero, Elisabete Machado, Rafael Cantón, Luísa Peixe, Teresa M. Coque
Ângela Novais
1Servicio de Microbiología, Hospital Universitario Ramón y Cajal, Madrid, Spain
2Unidad de Resistencia a Antibióticos y Virulencia Bacteriana asociada al Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain
3CIBER en Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
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Fernando Baquero
1Servicio de Microbiología, Hospital Universitario Ramón y Cajal, Madrid, Spain
2Unidad de Resistencia a Antibióticos y Virulencia Bacteriana asociada al Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain
3CIBER en Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
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Elisabete Machado
1Servicio de Microbiología, Hospital Universitario Ramón y Cajal, Madrid, Spain
4REQUIMTE, Laboratório de Microbiologia, Faculdade de Farmácia, Universidade do Porto, Porto, Portugal
5CEBIMED, Faculdade de Ciências da Saúde, Universidade Fernando Pessoa, Porto, Portugal
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Rafael Cantón
1Servicio de Microbiología, Hospital Universitario Ramón y Cajal, Madrid, Spain
2Unidad de Resistencia a Antibióticos y Virulencia Bacteriana asociada al Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain
3CIBER en Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
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Luísa Peixe
4REQUIMTE, Laboratório de Microbiologia, Faculdade de Farmácia, Universidade do Porto, Porto, Portugal
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Teresa M. Coque
1Servicio de Microbiología, Hospital Universitario Ramón y Cajal, Madrid, Spain
2Unidad de Resistencia a Antibióticos y Virulencia Bacteriana asociada al Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain
3CIBER en Epidemiología y Salud Pública (CIBERESP), Madrid, Spain
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  • For correspondence: mcoque.hrc@salud.madrid.org
DOI: 10.1128/AAC.00959-09
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  • FIG. 1.
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    FIG. 1.

    Characterization of multidrug resistance regions identified in the IncA/C2 plasmids carrying blaTEM-24. (A) In4-Tn402 and In0-Tn402 variants identified in pRYC103T24.1. (B) In4-Tn402 and In0-Tn402 variants identified in pRYC103T24.2. (C) The pRYC103T24.3 variant is similar to pRYC103T24.2, differing in the gene cassette array of In0-Tn402. Horizontal dotted lines represent the PCR mapping strategy used to characterize Tn402 derivatives and mercury resistance transposon operons. The locations of the primers used are indicated by white (In4-like variant) and black (In0 variant) triangles. Numbers represent primers described in Table 3 or the size (kb) of the PCR products. Open reading frames (ORFs) correspond to arrow-shaped boxes. Dark gray boxes represent transposition and mercury resistance modules, light gray boxes represent Tn402/class 1 integron derivatives, and cross-hatched boxes represent gene cassettes. The P1/Pant promoter type (In2/In4), which directs the expression of the gene cassettes, is shown. White circles symbolize 59-base elements of the corresponding gene cassettes. Rectangles correspond to insertion sequences (IS). Boxes bordered by a dotted line indicate incomplete or truncated ORFs. Arrows inside rectangles express the direction of transcription of the corresponding ORFs. Vertical bars symbolize inverted repeats of the integrons (IRi and IRt) and transposons (TIR). Horizontal bold lines show identity with highly similar regions (>99% identity) available in the GenBank database.

  • FIG. 2.
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    FIG. 2.

    Comparison of mercury resistance transposon platforms identified in different IncA/C plasmids. Tn402 derivatives and mercury resistance transposon derivatives found in the IncA/C plasmids pIP1202 (GenBank accession number CP000603), pSN254 (GenBank accession number CP000604), pCC416 (GenBank accession number AJ704863), and pRYC103T24.1 (GenBank accession numbers GQ293498 and GQ293499) (this study) are represented. Vertical bars represent the inverted repeats of integrons or transposons. Arrows inside boxes show the direction of transcription corresponding to different ORFs. Plasmid pSN254 contains two integrons in a “tail-to-tail” configuration; plasmid pCC416 has an integron lacking the 3′ CS region. Gene cassettes from pIP1202, pSN254, and pCC416 were similar to others described in the GenBank database: the aadA2 gene cassette was 100% homologous to that identified in plasmid pSAL-1 from Salmonella enterica serovar Enteritidis (GenBank accession number AJ237702); the aadA1 and aac3-VI genes were identical to those from IncA/C plasmids pAR060302, pAM4528, and peH4H, which probably are pSN254 derivatives (GenBank accession numbers FJ621588, FJ621587, and FJ621586, respectively), or the IncHI2 plasmid pAPEC-O1-R (GenBank accession number DQ517526). The blaVIM-4-aacA7-dfrA1-aadA1-smr array resembles that of the widespread In-e541 containing blaVIM-1 (GenBank accession number AJ870988) (13).

Tables

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  • TABLE 1.

    Amino acid changes, genetic environment, and plasmids associated with different TEM-2 derivatives among Enterobacteriaceae isolatesh

    TEM-type ESBLAlternative designationAmino acid substitution at positiona:blaTEM transposon/ genetic environmentPlasmid name (size [kb])Plasmid Inc groupIsolation yrSpeciesReference(s) (GenBank accession no.)
    21353992104153164182237238240244
    TEM-1abLDQGEHRAGERTn3Different conjugative and nonconjugative1963Multiple species 37, 45; http://www.lahey.org/studies (V00613)
    TEM-1bbTn2RSF1030 (48.5)Unknown1975c P. aeruginosa 27 (X54607)
    Tn2*dpDGO100, pRMH760IncC1978 E. coli 26, 46 (X54607, AY123253, AF188331, AF550679)
    TnSF1, p1658/97IncFII1997 K. pneumoniae
    Shigella flexneri
    TEM-1cb,eTn1_R7KeR7K (39.7)IncW1972 Providencia rettgeri 53
    TEM-2bKTn1IncA/C, IncC, IncF1965Multiple species (originally in E. coli) 30, 37 (L27758)
    RP1/RP4IncP1-α
    Tn1-Tn1696pCFF24 (85)fIncC1987 E. coli 30
    Tn801gRP1IncP1-α1969 P. aeruginosa 4, 28 (AF080442, AF466526)
    TEM-3CTX-1KKSTn1-Tn1696pCFF04 (85)fIncL/M1987 K. pneumoniae 30
    TEM-21KKRSIS6100-ΔTn801, IS4321-ΔTn801Chromosome, IncA/C21988 K. pneumoniae 19, 33
    M. morganii
    P. aeruginosa
    Alcaligenes faecalis
    TEM-8CAZ-2KKSSTn1-Tn1696pCFF34 (85)fIncL/M1987 K. pneumoniae 10, 30
    TEM-5CAZ-1STKNDpCFF14 (150)NI1987 K. pneumoniae 10
    TEM-24CAZ-6KKSTKTn1-Tn1696pCFF74 (85)f, pRYC103T24 (180)IncL/M IncA/C21988See introduction 3, 10, this study
    TEM-121CMT-4KKSTKSNDNINI2002 E. aerogenes 52
    TEM-16CAZ-7KKHNDpCFF84 (85)fIncL/M1988 K. pneumoniae 10, 30
    TEM-66KDKSND170-180NI1999c P. mirabilis 3
    TEM-7KSTn1-Tn1696ND (85)NI1988 C. freundii 30
    TEM-114KSTKNDNINI2001-2002 E. aerogenes 17
    TEM-67IKCTn1pANG-1 (48)NI1998 P. mirabilis, E. coli 40
    TEM-72KTSKNDpMN-13 (40), pPM-14 (40)NI1999 P. mirabilis, M. morganii 51
    • ↵ a Amino acid positions are numbered according to the Ambler et al. scheme (http://www.lahey.org/studies ).

    • ↵ b bla TEM-1a, blaTEM-1b, blaTEM-1c, and blaTEM-2 differ in the sequences corresponding to promoter and coding regions (24, 54).

    • ↵ c Publication date.

    • ↵ d A 1.516-kb sequence from Tn2* is identical to that available for the original Tn2 from RSF1030 (X54607), so Tn2 and Tn2* might be the same element. Four sequences highly similar to Tn2* are accessible in the GenBank database; three of them, pRMH760, TnSF1 (AF188331), and one side in p1658/97 (AF550679), had the same context, suggesting a common origin for this element (47).

    • ↵ e bla TEM-1c seems to result from homologous recombination between blaTEM-1a (from the promoter to the coding region up to position 345) and blaTEM-2 (from position 346 to the stop codon). This hybrid Tn1-Tn3 transposon was found in the IncW plasmid R7K, and it was named Tn1_R7K (54).

    • ↵ f These plasmids show identical sizes, restriction patterns, antibiotic resistance profiles (resistance to amikacin, kanamycin, netilmicin, tobramycin, tetracyclines, and sulfonamides), and presence of the aacA4 gene and belonged to the incompatibility group IncM or 7 (3, 10, 30). Although plasmid identification was not performed, they were similar to those encoding TEM-3 and TEM-24 in the same study (3). All of them share the ΔTn1-Tn1696 platform, suggesting a common origin (see the text).

    • ↵ g Tn801 is 97.7% similar to Tn3 at the nucleotide level; its transposase is 14 amino acids shorter at the N terminus than the Tn3 protein, and the repressors are identical. Although it was located in the early antibiotic IncP1-α plasmid RP1 recovered in the late 1960s, its sequence was determined later (4, 28, 44).

    • ↵ h ND, not determined; NI, not identified.

  • TABLE 2.

    Epidemiological data and plasmid characterization of multidrug-resistant TEM-24-producing Enterobacteriaceae isolatesg

    SpeciesPFGE typeaNo. of isolatesDate(s) (mo/yr)Origin (no. of isolates)Ward (no. of isolates)Sample type (no. of isolates)Non-β-lactam resistance profilebPlasmid Size (kb)cPlasmid Inc groupdRFLP pattern
    E. aerogenes EA7 8f11/98-07/04Spain (5)Med-ICU (2)Catheter (2)(Ak), Cp, Cm, Km, Na, (Nt), (Sm), Su, Tc, Tb, Tp180A/C2A
    France (2)Neurosurgery-ICUBlood (1)
    Portugal (1)Int medicineFecal (1)
    OutpatientWound (1)
    Unknown (2)Unknown (2)
    NephrologyBlood (1)
    E. aerogenes EA7A1 210/99-12/99SpainCV-ICUWound (1)(Ak), Cp, Cm, Km, Na, Nt, (Sm), Su, Tc, Tb, Tp180A/C2A
    BronchoscopyBAS (1)
    E. aerogenes EA7A3 311/02-12/02Portugal (2)Psychiatry (1)Urine (2)(Ak), (Cp), Cm, Km, Na, Nt, (Sm), Su, (Tc), Tb, Tp180A/C2A
    Int medicine (1)
    France (1)Nephrology (1)Blood (1)
    K. pneumoniae KP8 603/03-04/03PortugalBurn unit (3)Unknown (6)(Ak), Cm, Km, (Nt), (Sm), Su, (Tc), Tb, (Tp)180A/C2A
    Urology (1)
    Nephrology (1)
    Surgery (1)
    P. mirabilis PM1 201/03-04/03PortugalNeurosurgery (1)Urine (2)Ak, Cp, Cm, (Km), Na, (Nt), Sm, Su, Tc, (Tb), Tp180A/C2A
    Med-ICU (1)
    E. coli EC1 112/99SpainOutpatientBlood (1)Ak, Cp, Cm, Gm, Km, Na, Nt, Sm, Su, Tb, Tp180A/C2Ae
    EC2 103/00SpainOutpatientBlood (1)Cp, Cm, Km, Na, Nt, Sm, Su, Tc, Tb, Tp180A/C2A
    EC3 1f06/02SpainInt medicineNasal (1)Cp, Cm, Km, Na,Sm, Su, Tb, Tp180A/C2Ae
    EC4 1f06/02SpainNeurosurgeryRespiratory (1)Ak, Cp, Cm, Km, Nt, Sm, Su, Tb, Tp180A/C2A
    EC5 103/03PortugalNephrologyUrine (1)Ak, Cp, Cm, Km, Na, Nt, Sm, Su, Tc, Tb, Tp180A/C2
    EC6 103/03PortugalNeonatologyBlood (1)Ak, Km, Nt, Sm, Su, Tc, Tb, Tp180A/C2A
    K. oxytoca KO1103/04PortugalNeonatologyUnknown (1) Km, Nt, Su, Tb, Tp180, 151, 32A/C2ND
    • ↵ a Transferability of blaTEM-24 is indicated with underlining.

    • ↵ b Antibiotics for which there is resistance in transconjugants are underlined. Parentheses around antibiotics indicate variability among isolates. Transferability of the resistance to nalidixic acid cannot be evaluated, since the receptor strains used in conjugation assays are resistant to this antibiotic (E. coli BM21R Nalr Rifr).

    • ↵ c Plasmid size determined by hybridization of S1 nuclease-digested genomic DNA of E. coli BM21 transconjugants with a blaTEM-24 probe.

    • ↵ d Plasmids were characterized by identification of the incompatibility group by PCR, hybridization, and sequencing.

    • ↵ e Plasmids selected for the complete characterization of Tn402 and mercury resistance transposon derivatives.

    • ↵ f E. coli and E. aerogenes isolates recovered from the same patient (two cases).

    • ↵ g Abbreviations: Ak, amikacin; Cp, ciprofloxacin; Cm, chloramphenicol; Gm, gentamicin; Km, kanamycin; Na, nalidixic acid; Nt, netilmicin; Sm, streptomycin; Su, sulfonamide; Tc, tetracycline; Tb, tobramycin; Tp, trimethoprim; ICU, intensive care unit; CV-ICU, cardiovascular ICU; Med-ICU, medical ICU; Int medicine, internal medicine; ND, not determined.

  • TABLE 3.

    Oligonucleotides used in this study

    No.aPrimerSequence (5′-3′)GenBank accession no.Position (bp)Reference
    1TEM-FATGAGTATTCAACATTTCCG208-228 32
    2TEM-RCTGACAGTTACCAATGCTTA1075-1055 32
    3IR1 Tn21GGGTCGTCTCAGAAAACGGAF0714131-38 43
    4TnpR21 RATGCTATGCACCACCACGGAF0714133376-3394 43
    5TnpM21 RACAAGCGTCCGGTTTGACGAF0714133711-3728This study
    6TnpM21 FGTGTGGAAACACCCGACTGAF0714134020-4002This study
    7TnpA Tn1 RCCTTGTTAATCACCAGCCGTAM2617608755-8736This study
    85′CSGGCATCCAAGCAGCAAGAF1741291236-1252 43
    93′CSAAGCAGACTTGACCTGATAF1741292813-2830 43
    10IntI1FGGGTCAAGGATCTGGATTTCGAF0714134775-4755 32
    11IntI1RACATGCGTGTAAATCATCGTCGAF0714134312-4333 32
    12IntI2FCACGGATATGCGACAAAAAGGTL10818219-240 32
    13IntI2RGTAGCAAACGAGTGACGAAATGL108181007-986 32
    14IntI3FAGTGGGTGGCGAATGAGTGD50438178-196 32
    15IntI3RTGTTCTTGTATCGGCAGGTGD50438777-758 32
    16 aacA4 FTGACCTTGCGATGCTCTATGL068221440-1459This study
    17 aacA4 RCGGTACCTTGCCTCTCAAACL068221870-1851This study
    18 dfrA1 FATGGAGTGCCAAAGGTGAACAY9638032777-2796This study
    19 dfrA1 RGTTCACCTTTGGCACTCCATAY9638032709-2690This study
    20 cmlA1 RvGAATTGTGCTCGCTGTCGTAU123387095-7076This study
    21 qacEΔ1 RCAAGCTTTTGCCCATGAAGCAF0714136608-6589This study
    22orf5 FCGATATCGACGAGGTTGTGCAF0714137712-7730 43
    23orf5 RAGTTCTAGGCGTTCTGCGAF0714138157-8140 43
    24orf6 FCTTCCATCATCAACCCTGGATAU1233810315-10336This study
    25orf6 RTATCTTCGGCCTTCACACGU1233810486-10468This study
    26IS1326 FTACCGGGTCTTATGACCGAGTAF07141310357-10337 43
    27IS1326 RACTGTCATAGCGGTTCACGTTAF0714139141-9161 43
    28IS1326 FrAACGTGAACCGCTATGACAGTAF0714139161-9141 43
    29IS1353 FTGCAGCATTGTCTTGCGAGCAAF07141312113-12093 43
    30IS1353 RACACTACGGCAGCTGGGATAAF07141310830-10849 43
    31IS6100 FGGCTCTGTTGCAAAAATCGTGAAGAY4637974669-4692 43
    32IS6100 RGGCTCTGTTGCAAAGATTGGCAY4637975548-5528 43
    33IS5075 RTCGTCCAACTTTCGTTTCAACAY1966952699-2649This study
    34IS5075 FCGTGGGAAGGCCGTTTACCAY1966952155-2173This study
    35IS4321 RGCTAATAACGGCAGCTCCTCU6719410917-10936This study
    36 tniBΔ1 RAGCATCATCGGCTCGAAGCAF07141312588-12606 43
    37TniA FAGATGCGTGAGATTGTGACCAF07141313406-13387 43
    38TniA F2TCGTGCGGAGATCATCAGTCCAF07141314821-14801 43
    39TniA RGGACTGATGATCTCCGCACGAAF07141314801-14821 43
    40IRTTTTTCAGAAGACGACTGCACCAAF07141315034-15013This study
    41 merA1ACCATCGGCGGCACCTGCGTAF07141317597-17578 43
    42 merA5ACCATCGTCAGGTAGGGGAACAAAF07141316360-16382 43
    43 merR1696 RCCGGATGGTCTCCACATTGACU1233815904-15884This study
    44 sul2 FGCGCTAAGGCAGATGGCATTAY360321243-263This study
    45 sul2 RGCGTTTGATACCGGCACCCGTAY360321528-508This study
    46 strA FATTCTGACTGGTTGCCTGTCAM41223699552-99572This study
    47 strB RTAGATCGCGTTGCTCCTCTTAM412236101115-101095This study
    • ↵ a These numbers are referenced in Fig. 1.

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International Spread and Persistence of TEM-24 Is Caused by the Confluence of Highly Penetrating Enterobacteriaceae Clones and an IncA/C2 Plasmid Containing Tn1696::Tn1 and IS5075-Tn21
Ângela Novais, Fernando Baquero, Elisabete Machado, Rafael Cantón, Luísa Peixe, Teresa M. Coque
Antimicrobial Agents and Chemotherapy Jan 2010, 54 (2) 825-834; DOI: 10.1128/AAC.00959-09

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International Spread and Persistence of TEM-24 Is Caused by the Confluence of Highly Penetrating Enterobacteriaceae Clones and an IncA/C2 Plasmid Containing Tn1696::Tn1 and IS5075-Tn21
Ângela Novais, Fernando Baquero, Elisabete Machado, Rafael Cantón, Luísa Peixe, Teresa M. Coque
Antimicrobial Agents and Chemotherapy Jan 2010, 54 (2) 825-834; DOI: 10.1128/AAC.00959-09
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KEYWORDS

Anti-Bacterial Agents
DNA Transposable Elements
Drug Resistance, Multiple, Bacterial
Enterobacteriaceae
plasmids

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