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Bacteriology

Multi-Virulence-Locus Sequence Typing Identifies Single Nucleotide Polymorphisms Which Differentiate Epidemic Clones and Outbreak Strains of Listeria monocytogenes

Yi Chen, Wei Zhang, Stephen J. Knabel
Yi Chen
1Department of Food Science, The Pennsylvania State University, University Park, Pennsylvania 16802
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  • For correspondence: yxc211@psu.edu
Wei Zhang
2National Center for Food Safety and Technology, Illinois Institute of Technology, Summit, Illinois 60501
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Stephen J. Knabel
1Department of Food Science, The Pennsylvania State University, University Park, Pennsylvania 16802
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DOI: 10.1128/JCM.01575-06
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    FIG. 1.

    Unrooted neighbor-joining tree of 86 L. monocytogenes isolates based on the number of nucleotide differences in the six MVLST virulence gene fragments analyzed. Bootstrap values (1,000 replications) are shown at the interior branches. Lineage (i.e., I, II, and III) and serotype (i.e., 4b, 1/2a, and 1/2b) information for each isolate are included after the isolate identification number. Isolates described previously by Zhang et al. (60) were assigned new BL (Borland Laboratory) identification numbers and marked with asterisks in the figure.

Tables

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  • TABLE 1.

    Sources, lineages, and subtypes of the 66 representative isolates sequenced in this study

    Group and isolatePrevious IDaSourceaLineageaSerotypeaRibotypea,eMVLSTb
    Epidemic clone I (30)
        1981 Canada coleslaw outbreak* (WHOc, Health Canada)
            BL1301FSL J1-108HumanI4bDUP-1038B20
            BL1302FSL J1-107HumanI4dDUP-1038B20
            BL1303FSL J1-003HumanI4bDUP-1038B20
            BL1304FSL N3-008FoodI4bDUP-103820
        1985 California soft cheese outbreak* (WHO)
            BL1201FSL J1-002HumanI4bDUP-1038B20
            BL1202FSL J1-119HumanI4bDUP-1038B20
            BL1203FSL J1-110FoodI4bDUP-1038B20
        1983-1987 Switzerland soft cheese outbreak* (WHO)
            BL1101FSL J1-123HumanI4bDUP-1038B20
            BL1102FSL J1-126HumanI4bDUP-1038B20
            BL1103FSL N3-022FoodI4bDUP-1038B20
    Epidemic clone II (30)
        1998 Sara Lee hot dog outbreak (CDC)
            BL2101H2444NAdI4bDUP-104419
            BL2102H3396NAI4bDUP-104419
            BL2103H6383NAI4bDUP-104419
        2002 U.S. turkey deli outbreak (CDC)
            BL2201J1838NAI4bDUP-1044A19
            BL2202J2230NAI4bDUP-1044A19
            BL2203J2685NAI4bDUP-1044A19
            BL2204J3006NAI4bDUP-1044A19
            BL2205J3033NAI4bDUP-1044A19
            BL2206J3200NAI4bDUP-1044A19
            BL2207J3238NAI4bDUP-1044A19
    Epidemic clone III (30)
        2000 U.S. turkey deli outbreak* (CDC)
            BL3201FSL R2-603FoodII1/2aDUP-1053A1
            BL3202FSL R2-499FoodII1/2aDUP-1053A1
        1989 U.S. hot dog outbreak* (WHO)
            BL3101FSL N3-031FoodII1/2aDUP-1053A1
            BL3102FSL J1-101HumanII1/2aDUP-1053A1
    Epidemic clone IV (30)
        1989 United Kingdom pate outbreak* (WHO)
            BL4101FSL J1-129HumanI4bDUP-1042B21
            BL4102FSL J1-116HumanI4bDUP-1042B21
            BL4103FSL N3-013FoodI4bDUP-1042B21
        1979 Boston vegetable outbreak
            BL4201FSL J1-220HumanI4bDUP-104221
    Other outbreaks
        1983 Boston milk outbreak
            BL9101FSL J1-225HumanI4bDUP-1042B31
            BL9102FSL R2-578HumanI4bDUP-1042B31
            BL9103FSL R2-583HumanI4bDUP-1042B31
        2000 North Carolina soft cheese outbreak* (CDC)
            BL9201FSL R2-500FoodI4bDUP-1042B30
            BL9202FSL R2-501HumanI4bDUP-1042B30
        1987 Pennsylvania ice cream outbreak
            BL9301FSL J1-012HumanI4bDUP-1038B29
        1981 United Kingdom Carlisle outbreak
            BL9501FSL J1-105HumanII1/2aDUP-103033
        1994 Illinois chocolate milk outbreak* (WHO)
            BL9401FSL R2-502FoodI1/2bDUP-1051B32
            BL9402FSL R2-503HumanI1/2bDUP-1051B32
    Nonoutbreak isolates
        BL0002FSL N1-014FoodII1/2aNA34
        BL0003FSL N1-011AEnvironmentalI1/2bNA35
        BL00063562Food environmentNANADUP-104136
        BL00073563Food environmentNANADUP-104136
        BL0026FSL J2-044AnimalI4bDUP-104237
        BL0027FSL N3-010FoodI4bNA38
        BL00283564Food environmentNANADUP-104136
        BL0029FSL F2-239FoodI1/2bDUP-1042C39
        BL0030FSL F2-601Human sporadicI4bDUP-1042B40
        BL0031FSL H1-030Food environmentNANADUP-1045B41
        BL0032FSL F2-293FoodI1/2bDUP-1031A42
        BL0033FSL S4-436EnvironmentNANADUP-1025A43
        BL0034FSL H1-051Food environmentNANADUP-1039C44
        BL0035FSL L3-151Food environmentNANADUP-1039A45
        BL0036FSL F2-032FoodII1/2aDUP-1045B46
        BL0037FSL F2-373FoodII1/2aDUP-1039C47
        BL0038FSL N4-588EnvironmentNANADUP-1045B48
        BL0039FSL R2-219Food environmentNANADUP-1062A49
        BL0040FSL F3-831Food environmentNANADUP-1045A50
        BL0041FSL S6-016EnvironmentNANANA51
        BL0042FSL F2-525Human sporadicIII4bDUP-1061A52
        BL0043FSL F2-663Human sporadicII1/2aDUP-1054C53
        BL0044FSL C1-387FoodII1/2aDUP-1039B45
        BL0045FSL F2-695Human sporadicIII4aDUP-1061A54
        BL0046FSL F2-655Human sporadicIIINADUP-1061A55
        BL00473569Food environmentNANADUP-103056
        BL00483571Food environmentNANADUP-103945
        BL00493580Food environmentNANADUP-106257
        BL00503583Food environmentNANADUP-102358
    • ↵ a Isolates and information (sources, serotypes, ribotypes, and pulsotypes) were obtained from the Cornell Food Safety Laboratory, the U.S. CDC, and a meat-processing plant. ID, identification.

    • ↵ b Sequence types were assigned according to methods reported previously by Zhang et al. (60).

    • ↵ c Health agencies that characterized the outbreaks are included in parentheses following the name of the outbreaks. Isolates from the outbreaks followed by an asterisk were designated by the ILSI North America as a standard set of isolates for validating molecular subtyping methods.

    • ↵ d NA, not available.

    • ↵ e Ribotyping pattern designations followed by a capital letter indicate subribotype (i.e., DUP-1053A is a subribotype of ribogroup DUP-1053).

  • TABLE 2.

    Primer sequences, size of fragment, and percent coverage of complete coding sequence for each gene analyzed in this studya

    GeneSize of fragment (bp)Coverage of complete CDS (%)PCR and sequencing primers (5′-3′)Reference or source
    MVLST genes
        prfA46965.69AACGGGATAAAACCAAAACCA (F) 60
    TGCGATGCCACTTGAATATC (R)
        inlB43322.87CATGGGAGAGTAACCCAACC (F) 60
    GCGGTAACCCCTTTGTCATA (R)
        inlC41846.91CGGGAATGCAATTTTTCACTA (F) 60
    AACCATCTACATAACTCCCACCA (R)
        dal44141.10GGTTTCTGCGTAGCCATTTT (F) 60
    GGAAGGGGTCAATCCATACA (R)
        clpP41970.18CCAACAGTAATTGAACAAACTAGCC (F) 60
    GATCTGTATCGCGAGCAATG (R)
        lisR44865.70CGGGGTAGAAGTTTGTCGTC (F) 60
    ACGCATCACATACCCTGTCC (R)
    Additional virulence genes
        inlA45819.01GCTTTCAGCTGGGCATAAC (F)This study
    ATTCATTTAGTTCCGCCTGT (R)
        actA58232.01AAGAGGTAAATGCTTCGGACT (F)This study
    ATTCCATTTAGTTCCGCCTGT (R)
    • ↵ a CDS, coding sequence; F, forward; R, reverse.

  • TABLE 3.

    Nucleotide substitutions at the 28 nucleotide polymorphic sites in the six MVLST genes which were capable of differentiating all epidemiologically unrelated isolates analyzed in this study

    IsolateSNP locations in the six virulence genes
    prfA a inlB inlC dal clpP lisR
    ****************
    133233344124113433334
    8265921772214764195504812683
    3134038020177572345509538773
    ECIb C C C G C G A G T T C C G G C T A G C A G C C G C T G C
    ECII . . . . . . . . . . . . T A . C . . . . . T . . . . . .
    ECIII . T . . . . . . G C . T . . . . . T . G . T . . . . . T
    ECIV . . . . . . T A . . . . . . . . . . . . . . . . . . . .
    Boston milkb . . . . . . T A . . . . . . . . . . . . . . T . . . . .
    NC soft cheese T . . . T . . . . . . . T A . C . . . . . T . . . . . .
    PA ice cream . . . . . . . . . C . . T A . C . . . . . . . . . . . .
    IL milk . . . . T . . . G C . . T A . C . . . . . . . . . . . .
    United Kingdom Carlisle . . . A . A . . A C . . . . . . . T . G . T . . . . . .
    BL0002 . T . . . . . . G C . . T A . C . T . G . T . A . . . T
    BL0003 . . . . T . . . G . . . T A . C . . . . . . . . . G . T
    BL0004 . T . . . . . . G . . . . . T . . . . . . . . A T . . .
    BL0005 . . . . . . T A . . . . T A . C . . . . . T . . . . . .
    BL0008 . T . A . . . . A C . . . . . . . T . G . T . . . . . .
    BL0009 . T . A T . . . A C . T . . . . C T . G . T . . . . . T
    BL0010 . T . . . . T A . . . . . . . C . . . . A . . A T . . T
    BL0011 . . . . T . . . G C . . . A . C . . . . . T . . . . . T
    BL0012 . T . A T . . . A C . T . . . . . T . . . T . . . . . .
    BL0013 . T . A T . . . A C . . . . . . . T . G . T . . . . . .
    BL0014 . T . . . . . A . . . . . . . C C . . . . . . A T . . .
    BL0015 . . T . T . . . G C . . T A . C . . . . . T . . . . . .
    BL0016 . . . . T . . . G C . . . . . C . . . . . T . . . . . .
    BL0017 . T . . . A . . A C . . . . . . . . . G . T . . . . . .
    BL0018 . T . A . . . . G C . T . . T . . T . G . T . . . . . .
    BL0019 . T . A . A . . A C . T . . T . . T . G . T . . . . . .
    BL0020 . . T . T . . . G C . . . A . C . . . . . T . . . . . .
    BL0021 . T . . . . . . . . . . . . . C . . T . . . . A T . . .
    BL0022 . T . . . . . . G . . . . . . C . . . . . . . A T . . .
    BL0023 . T . . . . . A . . . T . . T . . . . . A . . A T . . .
    BL0024 . . . . . . . . . . . . . A . C . . . . . . . . . . . .
    BL0025 . . . . T . . . . . . . T A . C . . . . A T . . . . . .
    BL0026 . . . . . . T A . . T . . . . . . . . . . T . . . . . .
    BL0027 . . . . . . T A . . T . . . . . . . . . . . . . . . . .
    BL0028 . T . A T . . . A C . T . . . . . T . G . T . . . . . T
    BL0029 . . . . T . . . G . . . T A . C . . . . . . . . . . . .
    BL0030 . . . . T . . . . . . . T A . C . . T . . T . . . . . T
    BL0031 . T . A A . . A C . T . . T . . T . G . T . . T . . T
    BL0032 . . . . T . . . G C . . . . . . . . . . T . . . . . .
    BL0033 . . . . T . . . G C . . . . . . . . . G . T . . . . . .
    BL0034 . T . A . A . . G C . T . . T . . T . G . T . . T . . T
    BL0035 . T . A . . . . A C . T . . T . . T . G . T . . . . . T
    BL0036 . T . A . . . . G C . T . . . . . T . G . T . . . . . T
    BL0037 . T . A T . . . A C . T . . . . . T . G . T . . . . C T
    BL0038 . T . . . . . . G C . T . . . . . T . G . T . A T . . T
    BL0039 . . . . T . . . G C . . . . . . . . . . . T . . . . . T
    BL0040 . T . . . . . . G C . T . . T . . T . G . T . . . . . T
    BL0041 . T . A . . . . A C . T . . . . . T . G . T . . . . . T
    BL0042 . T . . . . . A . . . . . . . C C . . . A . . . T . . T
    BL0043 . . A . . . . A C . T . . T . . T . G . T . . . . . T
    BL0044 . T . A . . . . A C . T . . T . . T . G . T . . . . . T
    BL0045 . T . . . . . A . . . . . . . C C . . . A . . A T . . T
    BL0046 . T . . . . T A . . . . . . . C C . . . A . . A T . . T
    BL0047 . . A . A . . A C . T . . T . . T . G . T . . . . . T
    BL0048 . T . A . . . . A C . T . . T . . T . G . T . . . . . T
    BL0049 . T . A . A . . A C . T . . T . . T . G . T . . . . . T
    BL0050 . T . A . . . . A C . T . . T . . C . G . T . . . . . T
    • ↵ a Locations of the variable nucleotide sites in the virulence genes are shown by the numbers above. Position numbers that are in boldface and start with an asterisk represent the set of 16 nucleotide substitutions capable of differentiating all epidemic clones and outbreaks. Identical nucleotides at each polymorphic site are indicated by periods.

    • ↵ b All isolates within each epidemic clone or outbreak.

  • TABLE 4.

    Description analysis of nucleotide sequence data in all isolates, lineage I isolates, and outbreak isolates of serotype 4b

    IsolateGeneNo. of polymorphic sites% of polymorphic sitesNo. of synonymous mutationsNo. of nonsynonymous mutationsdN/dS ratioaπ/siteb
    All isolates prfA 388.103360.0150.017
    inlB 5312.2439150.0800.039
    inlC 368.3122140.1150.020
    dal 8419.0570140.0630.067
    clpP 409.553850.0200.028
    lisR 6314.15770.0040.031
    Lineage I isolates prfA 111.711010.0170.0033
    inlB 255.772050.1390.023
    inlC 30.72120.6050.004
    dal 71.36610.0740.048
    clpP 153.581320.0670.0005
    lisR 81.79530.0640.004
    Outbreak isolates of serotype 4b prfA 30.64210.0580.0015
    inlB 81.84530.3770.0036
    inlC 30.72120.5720.0017
    dal 51.13410.0740.0027
    clpP 00000
    lisR 30.67300.0028
    • ↵ a The dN/dS ratio was not calculated when the number of nonsynonymous mutations was zero.

    • ↵ b Average pairwise nucleotide difference per site.

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Multi-Virulence-Locus Sequence Typing Identifies Single Nucleotide Polymorphisms Which Differentiate Epidemic Clones and Outbreak Strains of Listeria monocytogenes
Yi Chen, Wei Zhang, Stephen J. Knabel
Journal of Clinical Microbiology Mar 2007, 45 (3) 835-846; DOI: 10.1128/JCM.01575-06

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Multi-Virulence-Locus Sequence Typing Identifies Single Nucleotide Polymorphisms Which Differentiate Epidemic Clones and Outbreak Strains of Listeria monocytogenes
Yi Chen, Wei Zhang, Stephen J. Knabel
Journal of Clinical Microbiology Mar 2007, 45 (3) 835-846; DOI: 10.1128/JCM.01575-06
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    • ABSTRACT
    • MATERIALS AND METHODS
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KEYWORDS

Disease Outbreaks
Listeria monocytogenes
listeriosis
Polymorphism, Single Nucleotide

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