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Mechanisms of Resistance

Six Groups of the OXY β-Lactamase Evolved over Millions of Years in Klebsiella oxytoca

Cindy Fevre, Mehdi Jbel, Virginie Passet, François-Xavier Weill, Patrick A. D. Grimont, Sylvain Brisse
Cindy Fevre
Unité Biodiversité des Bactéries Pathogènes Emergentes (U389 INSERM), Institut Pasteur, 25-28 rue du Dr Roux, 75724 Paris Cedex 15, France
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Mehdi Jbel
Unité Biodiversité des Bactéries Pathogènes Emergentes (U389 INSERM), Institut Pasteur, 25-28 rue du Dr Roux, 75724 Paris Cedex 15, France
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Virginie Passet
Unité Biodiversité des Bactéries Pathogènes Emergentes (U389 INSERM), Institut Pasteur, 25-28 rue du Dr Roux, 75724 Paris Cedex 15, France
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François-Xavier Weill
Unité Biodiversité des Bactéries Pathogènes Emergentes (U389 INSERM), Institut Pasteur, 25-28 rue du Dr Roux, 75724 Paris Cedex 15, France
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Patrick A. D. Grimont
Unité Biodiversité des Bactéries Pathogènes Emergentes (U389 INSERM), Institut Pasteur, 25-28 rue du Dr Roux, 75724 Paris Cedex 15, France
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Sylvain Brisse
Unité Biodiversité des Bactéries Pathogènes Emergentes (U389 INSERM), Institut Pasteur, 25-28 rue du Dr Roux, 75724 Paris Cedex 15, France
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  • For correspondence: sbrisse@pasteur.fr
DOI: 10.1128/AAC.49.8.3453-3462.2005
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  • FIG. 1.
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    FIG. 1.

    Phylogeny of the K. oxytoca β-lactamase gene. The neighbor-joining tree was rooted using as an outgroup the gene sequence of the SFO-1 β-lactamase (GenBank accession no. AB003148 ), the closest relative of blaOXY. Values at the nodes correspond to bootstrap values obtained after 1,000 replicates. Six major branches of K. oxytoca β-lactamase sequences are visible, corresponding to the blaOXY-1 to blaOXY-6β -lactamase gene groups.

  • FIG. 2.
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    FIG. 2.

    Phylogeny obtained based on 1,896 nt positions from the three housekeeping genes rpoB, gyrA, and gapDH. The neighbor-joining tree was rooted using K. pneumoniae type strain SB132 (= ATCC 13883T). Values at the nodes correspond to bootstrap values obtained after 1,000 replicates. Five branches of K. oxytoca are distinguished, corresponding to phylogenetic groups KoI to KoVI. blaOXY-5-harboring strains fall into the KoI branch.

Tables

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  • TABLE 1.

    K. oxytoca strains studied, β-lactamase (bla) gene sequences, housekeeping gene sequences, and their characteristicsa

    No.Strain name(s)Geographical sourceClinical sourcePhylogenetic groupbla groupbla accession no.Housekeeping gene accession no.
    rpoBgyrAgapDH16S rRNA
    Study isolates
        1SB9SpainBloodKoI (f) bla OXY-1 AJ871864 AJ871801 AJ303591 AJ871820 AJ871855
        2SB71FranceBloodKoI (f) bla OXY-1 AJ871865 AJ871802 AJ871839 AJ871821 AJ871856
        3SB136 (ATCC 49131)KoII (f) bla OXY-2 AJ871866 AJ871803 AF303608 AJ871822 AJ871857
        4SB175 (ATCC 13182T)KoII (f) bla OXY-2 AJ871867 AJ871804 AJ871840 AJ871823 AJ871858
        5SG271ClinicalKoIII bla OXY-3 (a) AF491278 (a) AJ871805 AJ871842 AJ871824 NDb
        6SG266ClinicalKoIV bla OXY-4 (a) AY077481 (a) AJ871806 AJ871841 AJ871825 ND
        7SB2908ItalyBloodKoI bla OXY-5 AJ871868 AJ871807 AJ871843 AJ871826 AJ871859
        8SB2909ItalyBloodKoI bla OXY-5 AJ871869 AJ871808 AJ871844 AJ871827 ND
        9SB2910ItalyBloodKoI bla OXY-5 AJ871870 AJ871809 AJ871845 AJ871828 ND
        10SB2933SwitzerlandBloodKoI bla OXY-5 AJ871871 AJ871810 AJ871846 AJ871829 ND
        11SB2942NetherlandBloodKoI bla OXY-5 AJ871872 AJ871811 AJ871847 AJ871830 AJ871860
        12SB73FranceWoundKoVI bla OXY-6 AJ871873 AJ871812 AJ871848 AJ871831 AJ871861
        13SB75GermanyBloodKoVI bla OXY-6 AJ871874 AJ871813 AJ871849 AJ871832 ND
        14SB324GermanyBloodKoVI bla OXY-6 AJ871875 AJ871814 AJ871850 AJ871833 ND
        15SB352FranceWoundKoVI bla OXY-8 AJ871876 AJ871815 AJ871851 AJ871834 ND
        16SB397South AfricaBloodKoVI bla OXY-6 AJ871877 AJ871816 AJ871852 AJ871835 ND
        17SB3037UkraineWoundKoVI bla OXY-6 AJ871878 AJ871817 AJ871853 AJ871836 AJ871862
        18SB3051FranceBloodKoVI bla OXY-6 AJ871879 AJ871818 AJ871854 AJ871837 AJ871863
    K. oxytoca c
        19SL781 (CIP104963)FranceKoI bla OXY-1 (b) Z30177 (b)NDNDNDND
        20SG12FranceKoI bla OXY-1 (a) AYO77482 (a)NDNDNDND
        21SG337FranceKoI bla OXY-1 (a) AYO77483 (a)NDNDNDND
        22SG49FranceKoI bla OXY-1 (a) AYO77486 (a)NDNDNDND
        23KH66SwedenKoI bla OXY-1 (c) Y17715 (c)NDNDNDND
        24E23004JapanKoI bla OXY-1 (d) M27459 (d)NDNDNDND
        25SG77FranceKoII bla OXY-2 (a) AY077488 (a)NDNDNDND
        26SG43FranceKoII bla OXY-2 (a) AY077487 (a)NDNDNDND
        27SG176FranceKoII bla OXY-2 (a) AY077485 (a)NDNDNDND
        28(CIP106098) SL911FranceKoII bla OXY-2 (b) Z49084 (b)NDNDNDND
        29SC10,436KoII bla OXY-2 (e) AY055205 (e)NDNDNDND
        30KH11SwedenKoII bla OXY-2 (c) Y17714 (c)NDNDNDND
    K. pneumoniae 31SB132 (ATCC 13883T)KpI bla SHV (g) AJ635407 (g) AJ871819 AF303606 (f) AJ875018 ND
    • ↵ a Phylogenetic groups, bla groups, and bla accession numbers followed by letter in parentheses were previously determined. References: a, 14; b, 11; c,31; d,1; e,15a; f,4; g,18. Other accession numbers correspond to sequences determined in this work.

    • ↵ b ND, not determined.

    • ↵ c Nucleotide sequences included for comparison.

  • TABLE 2.

    Primers, their sequences, and their positions on the gene

    Gene and primerSequencePositionsa
    bla
        OXY-E5′-GGT TTT GGT AAC TGT GAC GGG-3′−189 to −168
        OXY-G5′-CAG AGT GCA GAG TGT TGC AG-3′913 to 894
        OXY-H5′-GCG ACA ATA C(G/C)G CGA TGA-3′397 to 414
        OXY1-A5′-CGT GGC GTA AAA CCG CCC TG-3′14 to 33
        OXY1-B5′-GTC CGC CAA GGT AGC TAA TC-3′442 to 423
        OXY2-A5′-AAG GCT GGA GAT TAA CGC AG-3′285 to 304
        OXY2-B5′-GCC CGC CAA GGT AGC CGA TG-3′439 to 420
        OXY5-B5′-GAT TAA AAA AGC GGA TTT AGT A-3′297 to 318
        OXY5-C5′-GCC CGC CAA GGT AC CGA TA-3′442 to 423
        OXY6-B5′-CGG ATG ATT CGC AAA CCC TT-3′167 to 186
        OXY6-C5′-CGG GAT GGC TTT CGC TCT GC-3′274 to 255
    rpoB
        VIC25′-GGT TAC AAC TTC GAA GAC TC-3′2469 to 2489
        VIC35′-GGC GAA ATG GC(A/T) GAG AAC CA-3′1442 to 1422
    gyrA
        gyrA-A5′-CGC GTA CTA TAC GCC ATG AAC GTA-3′139 to 163
        gyrA-C5′-ACC GTT GAT CAC TTC GGT CAG G-3′762 to 741
    gapDH
        gapF-1735′-TGA AAT ATG ACT CCA CTC ACG G-3′135 to 153
        gapR-1815′-CTT CAG AAG CGG CTT TGA TGG CTT-3′771 to 747
    rrs
        Ad5′-AGA GTT TGA TCM TGG CTC AG-3′8 to 27
        rJ5′-GGT TAC CTT GTT ACG ACT T-3′1508 to 1491
        D5′-CAG CAG CCG CGG TAA TAC-3′518 to 535
        E5′-ATT AGA TAC CCT GGT AGT CC-3′786 to 805
        rE5′-GGA CTA CCA GGG TAT CTA AT-3′805 to 786
    • ↵ a The first position refers to the start codon, exept for the rrs sequences, for which the first position corresponds to the first nucleotide of the sequence available under accession number Y01859 in the GenBank database.

  • TABLE 3.

    Amino acid sequence variation among OXY-1 to OXY-6 β-lactamase (bla) groups

    Strainbla alleleaEnzymeapIAmino acid at position (Ambler no.):Amino acid at position (Ambler no.):Amino acid at position (Ambler no.):Amino acid at position (Ambler no.):
    249 (5)11 (7)12 (8)15 (11)16 (12)17 (13)22 (18)24 (20)25 (21)29 (25)30 (26)31 (27)32 (28)33 (29)34 (30)38 (34)39 (35)43 (39)44 (40)54 (50)56 (52)58 (54)61 (56)75 (72)90 (87)91 (88)92 (89)101 (98)102 (99)103 (100)111 (108)129 (126)140 (137)141 (138)143 (140)156 (153)161 (158)168 (165)171 (168)174 (171)180 (177)184 (181)194 (190)200 (197)230 (227)233 (230)240 (237)256 (255)261 (260)262 (261)270 (269)275 (274)278 (277)
    SL781 bla OXY-1-1a OXY-1-17.5bLSTLMAAVAGSSADAIQADRSNADTGNPEKKSIAKMSQVTASKTRNAAANVLQSE
    SB71 bla OXY-1-2a OXY-1-27.7VG
    SB9 bla OXY-1-2a OXY-1-27.7VG
    SG12 bla OXY-1-3a OXY-1-3NAcG
    SG337 bla OXY-1-4a OXY-1-4NADeldV
    SG49 bla OXY-1-5a OXY-1-5NAVG
    KH66 bla OXY-1-6a OXY-1-65.25bPK
    E23004 bla OXY-1-7a OXY-1-77.4b
    SG271 bla OXY-3-1a OXY-3-16.7bITSIDelLCSDelDelNSTDTNIKDAVGRTEHVLD
    SG266 bla OXY-4-1a OXY-4-17.7bSDelTLHDIGMG
    SB2908 bla OXY-5-1a OXY-5-17.2DelHTAIGM
    SB2909 bla OXY-5-1a OXY-5-17.2DelHAIGM
    SB2910 bla OXY-5-1a OXY-5-17.2DelHAIGM
    SB2942 bla OXY-5-1a OXY-5-17.2DelHAIGM
    SB2933 bla OXY-5-2a OXY-5-27.7DelAIGLM
    SB73 bla OXY-6-1a OXY-6-17.75SHD
    SB75 bla OXY-8-1a OXY-6-17.75SHD
    SB324 bla OXY-6-2a OXY-6-27.75SDelHD
    SB352 bla OXY-5-3a OXY-6-37.75STHD
    SB397 bla OXY-6-4a OXY-6-48.1SNHD
    SB3037 bla OXY-6-4a OXY-6-48.1SNHD
    SB3051 bla OXY-6-4a OXY-6-48.1SNHD
    SB136 bla OXY-2-1a OXY-2-1NAIIMLDelATHTNISKNAATLIGHATTESDEVDN
    SB175 bla OXY-2-2a OXY-2-2NAIIMLDelATHTNISKNAATLIGRATTESDEVDIN
    SG77 bla OXY-2-3a OXY-2-3NAIIMLDelDelATHTNISKNAATLIGRATTESDEVGDIN
    KH11 bla OXY-2-4a OXY-2-4NAIIMLDelDelATHTNISKNAATLIGRATTESDEVDN
    SG43 bla OXY-2-5a OXY-2-5NAIIMLDelDelATHTNISKNAATLIGRATTESDEVDN
    SG176 bla OXY-2-6a OXY-2-6NAIIMLDelSATHTNISKNAATLIGRATTESDEVDN
    SL911 bla OXY-2-7a OXY-2-7NAIIMLDelATHTNISKNAATLIGRATTESDEVDN
    SC10,436 bla OXY-2-8a OXY-2-8NAIIMLDelSATHTNISKNAATLIGRATTESAEVN
    • ↵ a Numbered in this study.

    • ↵ b Value from the literature.

    • ↵ c NA, not available.

    • ↵ d Del, deletion.

  • TABLE 4.

    Percent average nucleotide and aminoacid β-lactamase sequence similarity within and among bla OXY groupsa

    Group (no. of strains)Avg % similarity (SD)
    blaOXY-1blaOXY-2blaOXY-3blaOXY-4blaOXY-5blaOXY-6
    bla OXY-1 (8)99.7 (0.09)/99.4 (0.4)87.2 (2.3)86.2 (5)95.2 (1.7)97.5 (0.5)97.1 (0.5)
    bla OXY-2 (8)89.5 (0.4)99.7 (0.1)/99.4 (0.4)84.9 (5.6)86.2 (5)87 (2.9)86.5 (2.6)
    bla OXY-3 (1)90.9 (0.2)88.6 (0.5)100 (0)/100 (0)86.3 (0.0)85.1 (6.7)85.6 (5.6)
    bla OXY-4 (1)96.8 (0.3)88.3 (0.3)90 (0)100 (0)/100 (0)95.9 (1.7)95.6 (0.1)
    bla OXY-5 (5)97.5 (0.3)91.5 (0.3)90.3 (0)97.2 (0.4)99.8 (0.1)/99.7 (0.4)95.8 (1)
    bla OXY-6 (7)98.3 (0.3)88.7 (0.3)91.2 (0.3)97.7 (0.2)97 (0.2)99.8 (0.1)/99.7 (0.2)
    • ↵ a Above diagonal, nucleotide sequence similarity; below diagonal, amino acid sequence similarity; inside diagonal cells: nucleotide/amino acid sequence similarities.

  • TABLE 5.

    MICs of 10 β-lactams and threeβ -lactam-β-lactam inhibitor combinations observed for strains harboring blaOXY-1 to blaOXY-6 β-lactamase genes

    Drug(s)MIC (μg/ml)
    blaOXY-1 strains SB9, SB71blaOXY-2 strains SB136, SB175blaOXY-3 strains SG271ablaOXY-4 strains SG266ablaOXY-5 strains SB2908, SB2933blaOXY-6 strains SB73, SB324, SB352, SB397
    Amoxicillin2565121664256256
    Amoxicillin + 2 μg/ml of clavulanate440.250.542-4
    Ticarcillin128128166412864-128
    Ticarcillin + 2 μg/ml of clavulanate220.5221-2
    Piperacillin16-3216-32128-328-32
    Piperacillin + 4 μg/ml of tazobactam21-20.120.52-42-4
    Cephalothin4-816222-44-8
    Cefoxitin4-820.512-84-8
    Cefotaxime≤0.06≤0.06-0.125≤0.06≤0.06≤0.06≤0.06
    Ceftazidime0.125-0.250.125-0.25≤0.06≤0.060.125-0.250.25-0.5
    Cefepime≤0.06≤0.06-0.125≤0.06≤0.06≤0.06≤0.06
    Aztreonam≤0.06-0.250.25≤0.06≤0.06≤0.06-0.125≤0.06-0.25
    Imipenem0.1250.1250.50.50.1250.125
    • ↵ a Values previously published (14).

  • TABLE 6.

    Nucleotide polymorphism observed among the 18 study isolates

    GeneFragment size (bp)No. of variable sites (%)No. of substitutions (%)
    SingletonInformativeTotalSynonymousNonsynonymousTotal
    rpoB 94034 (3.6)48 (5.1)82 (8.7)82 (8.7)5 (0.5)87 (9.3)
    gyrA 38315 (3.9)17 (4.4)32 (8.4)33 (8.6)1 (0.3)34 (8.9)
    gapDH 57326 (4.5)13 (2.3)39 (6.8)38 (6.6)3 (0.5)41 (7.2)
    bla 870, 873, or 87664 (7.3)139 (15.9)203 (23.2)158 (18.0)52 (5.9)210 (24.0)
  • TABLE 7.

    Percent average rpoB, gyrA, and gapDH nucleotide sequence divergence within and among the five K. oxytoca phylogenetic groups and clone blaOXY-5

    Group or cloneAvg % divergence from nucleotide sequence
    KoIKoIIKoIIIKoIVblaOXY-5 cloneKoVI
    rpoBgyrAgapDHrpoBgyrAgapDHrpoBgyrAgapDHrpoBgyrAgapDHrpoBgyrAgapDHrpoBgyrAgapDH
    KoI0.20.503.093.21.924.254.964.363.23.650.70.490.520.003.042.680.67
    KoII0.110.1304.155.095.44.153.262.4433.131.923.62.682.24
    KoIIINAaNANA4.365.484.884.324.74.364.324.514.51
    KoIVNANANA2.833.650.72.961.30.67
    bla OXY-5 clone0.170.000.063.12.420.67
    KoVI0.40.130.1
    • ↵ a NA, not applicable (only one sequence per group).

  • TABLE 8.

    Average numbers of synonymous substitutions per synonymous site (Ks values) among the five K. oxytoca phylogenetic groups and clone blaOXY-5a

    Group or cloneAvg Ks value
    KoIKoIIKoIIIKoIVClone blaOXY-5KoVI
    KoI0.1140.170.1280.020.12
    KoII0.1350.1570.1560.1110.133
    KoIII0.210.2140.1750.1730.171
    KoIV0.1430.1260.220.1130.117
    Clone blaOXY-50.0220.1320.1990.1430.123
    KoVI0.1120.1280.1880.0450.101
    • ↵ a Data computed from gene rpoB (above diagonal) and gyrA (below diagonal).

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Six Groups of the OXY β-Lactamase Evolved over Millions of Years in Klebsiella oxytoca
Cindy Fevre, Mehdi Jbel, Virginie Passet, François-Xavier Weill, Patrick A. D. Grimont, Sylvain Brisse
Antimicrobial Agents and Chemotherapy Jul 2005, 49 (8) 3453-3462; DOI: 10.1128/AAC.49.8.3453-3462.2005

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Six Groups of the OXY β-Lactamase Evolved over Millions of Years in Klebsiella oxytoca
Cindy Fevre, Mehdi Jbel, Virginie Passet, François-Xavier Weill, Patrick A. D. Grimont, Sylvain Brisse
Antimicrobial Agents and Chemotherapy Jul 2005, 49 (8) 3453-3462; DOI: 10.1128/AAC.49.8.3453-3462.2005
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KEYWORDS

Evolution, Molecular
Klebsiella oxytoca
beta-lactamases

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