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Mechanisms of Resistance

Characterization of a New Metallo-β-Lactamase Gene, blaNDM-1, and a Novel Erythromycin Esterase Gene Carried on a Unique Genetic Structure in Klebsiella pneumoniae Sequence Type 14 from India

Dongeun Yong, Mark A. Toleman, Christian G. Giske, Hyun S. Cho, Kristina Sundman, Kyungwon Lee, Timothy R. Walsh
Dongeun Yong
1Yonsei University College of Medicine, Research Institute of Antimicrobial Resistance, Seoul, Republic of Korea
2Department of Medical Microbiology, Cardiff University, Cardiff, United Kingdom
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Mark A. Toleman
2Department of Medical Microbiology, Cardiff University, Cardiff, United Kingdom
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Christian G. Giske
3Clinical Microbiology, MTC—Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden
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Hyun S. Cho
4Yonsei University College of Life Science and Biotechnology, Seoul, Republic of Korea
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Kristina Sundman
5Department of Clinical Microbiology, Örebro University Hospital, Örebro, Sweden
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Kyungwon Lee
1Yonsei University College of Medicine, Research Institute of Antimicrobial Resistance, Seoul, Republic of Korea
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Timothy R. Walsh
2Department of Medical Microbiology, Cardiff University, Cardiff, United Kingdom
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  • For correspondence: WalshTR@Cardiff.ac.uk
DOI: 10.1128/AAC.00774-09
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  • FIG. 1.
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    FIG. 1.

    Alignment of novel erythromycin esterase EreC (this study) with EreA and EreA2. Amino acid changes between EreC and EreA are indicated with asterisks. The single amino acid difference between EreA and EreA2 is highlighted in gray.

  • FIG. 2.
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    FIG. 2.

    Three characterized antibiotic resistance-conferring regions from K. pneumoniae 05-506. (A) The 4.3-kb region is linked to the 4.8-kb complex class 1 integron region. The genes encoding the efflux pump and lactate dehydrogenase (gray diagonal lines) are of Klebsiella origin. blaNDM-1 (dark gray) is flanked between the pathogenicity island (vertical black lines) and IS26/Tn3 (black small squares). This region lies downstream of the 4.8-kb complex class 1 integron containing Int (checkered area), arr-2, ere2A, aadA1, and cmlA7 as gene cassettes and qacΔ1 (white boxes). Downstream is an intact copy of ISCR1 (black and white diagonal lines). Arrows, direction of transcription; black ellipses, 59-base elements; Δ, genes that are truncated. (B) blaCMY-4 (gray) is located between ISEcP1 (black) and blc (white), as reported previously (16).

  • FIG. 3.
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    FIG. 3.

    Alignment of the amino acid sequences of NDM-1 with the amino acid sequences of IMP-1, IMP-2, IMP-8, VIM-1, VIM-2, GIM-1, SPM-1, SIM-1, and KHM-1. Conserved residues coordinating zinc ions are denoted with asterisks. Key amino acids are also numbered according to the BBL scheme (12). Additional amino acids unique to NDM-1 are enclosed in a light gray box. Amino acid substitutions near the active site are highlighted in plain boxes (13).

  • FIG. 4.
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    FIG. 4.

    Phylogenetic tree obtained for MBL subgroup B1. The numbers for the substitutions should be multiplied by 100. The alignment used was prepared with the CLUSTALW program. The GenBank accession numbers for the sequences are as follows: IMP-1, S71932; IMP-2, AJ243491; IMP-8, AF322577; VIM-1, Y18050; VIM-2, AF191564; GIM-1, AJ620678; SPM-1, AJ492820; SIM-1, AY887066; KHM-1, AB364006.

  • FIG. 5.
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    FIG. 5.

    PFGE of plasmids from K. pneumoniae 05-506, conjugant E. coli J53(pNDM-1), and E. coli NF-NDM-1 (from the patient's normal flora). The bands with white arrows showed positive signals by Southern blot hybridization with the NDM-1 probe (data nor shown). K. pneumoniae 05-506 carries blaNDM-1 on a 180-kb plasmid, whereas E. coli NF-NDM-1 carries blaNDM-1 on a plasmid of approximately 140 kb.

  • FIG. 6.
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    FIG. 6.

    PFGE findings (A and C) and Southern blot hybridization (B and D) with blaNDM-1 (A and B) and an ISCR1 probe (C and D). The genomic DNA of the index strain (K. pneumoniae 05-506) was undigested (lane 1) or was digested with S1 nuclease (lane 2), XbaI (lane 4), SpeI (lane 5), or I-CeuI (lane 6). Lane 3, DNA size marker.

Tables

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  • TABLE 1.

    Antimicrobial susceptibility patterns of K. pneumoniae 05-560, E. coli NF-NDM-1, transformants, and conjugants

    AntibioticMIC (μg/ml)
    K. pneumoniae 05-560E. coli TOP10E. coli TOP10(NDM-1)E. coli J53E. coli J53(pNDM-1)E. coli NF-NDM-1
    Ampicillin>25612>2564>256>256
    Piperacillin>2560.5NT1>256>256
    Cephalothin>2568>2564>256>256
    Cefoxitin>2564>2562>256>256
    Cefotaxime>2560.125>2560.064>256>256
    Cefuroxime>2568>2568>256>256
    Ceftazidime>2561>2560.125>256>256
    Aztreonam>2560.0940.250.0642424
    Cefepime>2560.03280.0642424
    Ertapenem>320.125240.5>32>32
    Imipenem>320.094120.2516>32
    Meropenem>320.064120.064>32>32
    Ciprofloxacin>320.0040.0060.0320.0474
    Colistin0.750.380.380.250.250.25
  • TABLE 2.

    Steady-state kinetic constants of NDM-1, IMP-1, and VIM-2

    CompoundNDM-1IMP-1aVIM-2b
    Km (μM)kcat (s−1)kcat/Km (s−1/μM)Km (μM)kcat (s−1)kcat/Km (s−1/μM)Km (μM)kcat (s−1)kcat/Km (s−1/μM)
    Penicillin G16110.685203200.6249561.14
    Ampicillin22150.662009504.8DNA
    Piperacillin12141.17NDcNDND72330.45
    Cephalothin1040.4021482.444571.28
    Cefoxitin4910.0281622430.12
    Cefotaxime1060.5841.30.3532280.86
    Cefuroxime850.613780.2222120.55
    Ceftazidime18150.034480.1898890.90
    AztreonamND>1,000>0.01<0.0001ND<0.5ND
    Cefepime77130.171170.6618450.03
    Imipenem94200.2139461.210100.99
    Meropenem49120.2510500.12510.28
    Clavulanic acidNDNRdNR
    • ↵ a From Spencer et al. (32).

    • ↵ b From Poirel et al. (23).

    • ↵ c ND, not detected.

    • ↵ d NR, not reported.

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Characterization of a New Metallo-β-Lactamase Gene, blaNDM-1, and a Novel Erythromycin Esterase Gene Carried on a Unique Genetic Structure in Klebsiella pneumoniae Sequence Type 14 from India
Dongeun Yong, Mark A. Toleman, Christian G. Giske, Hyun S. Cho, Kristina Sundman, Kyungwon Lee, Timothy R. Walsh
Antimicrobial Agents and Chemotherapy Nov 2009, 53 (12) 5046-5054; DOI: 10.1128/AAC.00774-09

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Characterization of a New Metallo-β-Lactamase Gene, blaNDM-1, and a Novel Erythromycin Esterase Gene Carried on a Unique Genetic Structure in Klebsiella pneumoniae Sequence Type 14 from India
Dongeun Yong, Mark A. Toleman, Christian G. Giske, Hyun S. Cho, Kristina Sundman, Kyungwon Lee, Timothy R. Walsh
Antimicrobial Agents and Chemotherapy Nov 2009, 53 (12) 5046-5054; DOI: 10.1128/AAC.00774-09
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KEYWORDS

Carboxylic Ester Hydrolases
Klebsiella Infections
Klebsiella pneumoniae
beta-lactamases

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