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Bacteriology

Comparison of Single- and Multilocus Sequence Typing and Toxin Gene Profiling for Characterization of Methicillin-Resistant Staphylococcus aureus

Yongwei Cai, Fanrong Kong, Qinning Wang, Zhongsheng Tong, Vitali Sintchenko, Xianyu Zeng, Gwendolyn L. Gilbert
Yongwei Cai
1Centre for Infectious Diseases and Microbiology (CIDM), Institute of Clinical Pathology and Medical Research (ICPMR), Westmead, New South Wales, Australia
2Department of Dermatology, Hangzhou Third People's Hospital, Hangzhou, Zhejiang Province, People's Republic of China
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Fanrong Kong
1Centre for Infectious Diseases and Microbiology (CIDM), Institute of Clinical Pathology and Medical Research (ICPMR), Westmead, New South Wales, Australia
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Qinning Wang
1Centre for Infectious Diseases and Microbiology (CIDM), Institute of Clinical Pathology and Medical Research (ICPMR), Westmead, New South Wales, Australia
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Zhongsheng Tong
1Centre for Infectious Diseases and Microbiology (CIDM), Institute of Clinical Pathology and Medical Research (ICPMR), Westmead, New South Wales, Australia
3Research Laboratory for Infectious Skin Diseases, Department of Dermatology, Wuhan First Hospital, Wuhan 430022, People's Republic of China
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Vitali Sintchenko
1Centre for Infectious Diseases and Microbiology (CIDM), Institute of Clinical Pathology and Medical Research (ICPMR), Westmead, New South Wales, Australia
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Xianyu Zeng
3Research Laboratory for Infectious Skin Diseases, Department of Dermatology, Wuhan First Hospital, Wuhan 430022, People's Republic of China
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Gwendolyn L. Gilbert
1Centre for Infectious Diseases and Microbiology (CIDM), Institute of Clinical Pathology and Medical Research (ICPMR), Westmead, New South Wales, Australia
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  • For correspondence: lyng@icpmr.wsahs.nsw.gov.au
DOI: 10.1128/JCM.01082-07
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  • FIG. 1.
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    FIG. 1.

    Relatedness of 42 MRSA strains between different typing methods. *, strains CH 69, IPO1M2046, and 14176-5710 belonged to spa types t1963, t1958, and t1959, respectively, which have not been previously deposited in the database.

  • FIG. 2.
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    FIG. 2.

    The 13 toxin gene profiles of the 41 strains. Lanes 1 to 42 show results for the following isolates, in order (see Table 1): FH43, SJOG 30, RPH85, B827549, SN39, RHH58, RHH10, FH53, B8-10, RPH2, IMVS67, CH16, CH69, PAH58, PAH1, E822485, J710566, RPH74, E804531, CH97, IP01M2046, C801535, F829549, RBH98, 13792-4492, IP01M1081, 14176-5710, K704540, K711532, AH13, RDH81, AH1, RPAH18, RPAH15, COL, MW2, DEN2988, BK2464, HDG2, HU25, a control strain, and ANS46.

Tables

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  • TABLE 1.

    Genotypes and spa types of 42 well-characterized methicillin-resistant S. aureus isolates used in this study

    StrainGenBank accession no.aDefined spa lengthbspa typecspa profilecClonal typed, eSources of Australian isolatesh
    B827549EF094508134t178407-34-33-13ST∼1-SCCmec-newQHPS
    HU25gEF094528182t13808-16-02-25-17-24ST239-SCCmec-IIIA
    HDG2gEF094527182t42115-12-16-02-25-17ST239-SCCmec-IIIB
    K704540fEF094525206t03715-12-16-02-25-17-24ST∼239-SCCmec-IIIQHPS
    K711532f= EF094525206t03715-12-16-02-25-17-24ST∼239-SCCmec-IIIQHPS
    AH13f= EF094525206t03715-12-16-02-25-17-24ST239-SCCmec-IIIAAGAR
    RDH81f= EF094525206t03715-12-16-02-25-17-24ST239-SCCmec-IIIAAGAR
    AH1f= EF094525206t03715-12-16-02-25-17-24ST128-SCCmec-IIIAAGAR
    RPAH 18f= EF094525206t03715-12-16-02-25-17-24ST239-SCCmec-IIIAGAR
    RPAH15f= EF094525206t03715-12-16-02-25-17-24ST239-SCCmec-IIIAGAR
    ANS46g= EF094525206t03715-12-16-02-25-17-24ST239-SCCmec-III
    PC8fEF094507206t12707-23-21-16-34-33-13ST1-SCCmec-IVAGAR
    FH43f= EF094507206t12707-23-21-16-34-33-13ST∼1-SCCmec-IVAGAR
    SJOG 30f= EF094507206t12707-23-21-16-34-33-13ST1-SCCmec-IVAGAR
    RPH 85f= EF094507206t12707-23-21-16-34-33-13ST∼1-SCCmec-IVAGAR
    SN39f= EF094507206t12707-23-21-16-34-33-13ST∼1-SCCmec-newAGAR
    RHH58f= EF094507206t12707-23-21-16-34-33-13ST∼1-SCCmec-IVAGAR
    RHH10f= EF094507206t12707-23-21-16-34-33-13ST∼1-SCCmec-IVAGAR
    FH53f= EF094507206t12707-23-21-16-34-33-13ST∼1-SCCmec-IAGAR
    RPH2fEF094510206t19011-17-34-24-34-22-25ST8-SCCmec-newAGAR
    PAH 58fEF094514230t01908-16-02-16-02-25-17-24ST30-SCCmec-IVAGAR
    PAH 1f= EF094514230t01908-16-02-16-02-25-17-24ST30-SCCmec-IVAGAR
    MW2gEF094526230t12807-23-23-21-16-34-33-13ST1-SCCmec-IV
    RBH98fEF094522230t20211-17-23-17-17-16-16-25ST93-SCCmec-IVAGAR
    13792-4492f= EF094522230t20211-17-23-17-17-16-16-25ST∼93-SCCmec-IVQHPS
    IP01M1081fEF094523230t21604-20-17-20-17-31-16-34ST59-SCCmec-IVQHPS
    14176-5710fEF094524230t1959c15-21-12-16-02-25-17-16ST∼239-SCCmec-IIIQHPS
    B8-10fEF094509230t71104-21-17-34-24-34-22-25ST∼8-SCCmec-IVQHPS
    J710566fEF094516254t06509-02-16-34-13-17-34-16-34ST45-SCCmec-VQHPS
    RPH 74fEF094517254t12309-02-16-34-13-16-34-16-34ST45-SCCmec-VAGAR
    IP01M2046fEF094519254t1958c08-21-17-13-13-new-34-33-34ST78-SCCmec-IVQHPS
    E804531fEF094518278t00226-23-17-34-17-20-17-12-17-16ST5-SCCmec-IVQHPS
    CH97f= EF094518278t00226-23-17-34-17-20-17-12-17-16ST73-SCCmec-IVAGAR
    BK2464g= EF094518278t00226-23-17-34-17-20-17-12-17-16ST5-SCCmec-II
    IMVS 67fEF094511278t00811-19-12-21-17-34-24-34-22-25ST8-SCCmec-VAGAR
    COLg= EF094511278t00811-19-12-21-17-34-24-34-22-25ST250-SCCmec-I
    DEN2988g= EF094511278t00811-19-12-21-17-34-24-34-22-25ST8-SCCmec-IVA
    F829549fEF094521278t18607-12-21-17-13-13-34-34-33-34ST88-SCCmec-IVQHPS
    C801535fEF094520278t32507-12-21-17-34-13-34-34-33-34ST88-SCCmec-newQHPS
    E822485fEF094515302t01815-12-16-02-16-02-25-17-24-24-24ST36-SCCmec-IIQHPS
    CH69fEF094513326t1963c26-23-13-17-31-29-17-25-17-25-16-28ST∼22-SCCmec-IVAGAR
    CH16fEF094512422t03226-23-23-13-23-31-29-17-31-29-17-25-17-25-16-28ST22-SCCmec-IVAGAR
    • ↵ a The relevant spa sequences have been submitted to GenBank; other strains with identical spa sequences are indicated by “=” and the accession no. for the corresponding submitted GenBank sequence.

    • ↵ b Defined spa lengths are the distances from the start and end points, equal to 1156 and 1481 in GenBank sequence J01786, which correlates with the start and end point of the suggested 5′ and 3′ signature sequences (www.spaServer.Ridom.de ). The full repetitive region sequence length can be calculated by adding together the lengths of sequences of individual repeats.

    • ↵ c After comparison with spa database (www.spaServer.Ridom.de ) and GenBank sequences, three new spa types sequences were identified and submitted to the spa database (www.spaServer.Ridom.de ). Please refer to the spa database for spa type and profile nomenclature.

    • ↵ d ST, MLST; SCCmec, staphylococcal cassette chromosome mec. Information provided by strain donors; ST∼, single nucleotide polymorphism type as described by Huygens et al. (18) using the computer program Minimum SNPs to compare with existing MLST data (17).

    • ↵ e Clonal type refers to the combination of ST and SCCmec type.

    • ↵ f Thirty-five Australian strains were provided by Philip Giffard, Cooperative Research Centre for Diagnostics, Queensland University of Technology, Brisbane, Australia, and Graeme Nimmo, Queensland Health Pathology Services, Princess Alexandra Hospital, Brisbane, and have been used in several previous studies (17, 18, 40).

    • ↵ g Seven isolates were provided by Herminia de Lencastre, Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Oeiras, Portugal, and have been used in several previous studies (33, 34); spa types identified in this study were identical with those previously reported for these strains (de Lencastre, personal communication).

    • ↵ h QHPS, Queensland Health Pathology Service (isolates from various diagnostic laboratories in Queensland); AGAR, Australian Group on Antibiotic Resistance (isolates from a study of community MRSA in Australia) (6).

  • TABLE 2.

    Primers and probes used in mPCR/RLB for detection of 13 toxin genes

    Primer/probeaTargetTm °CbGenBank accession no.Primer/probe sequence (5′-3′)cReferencesd
    nucSb nuc 65.68V01281 511GCG ATT GAT GGT GAT ACG GTT531 7
    nucAp nuc 61.36V01281 558CAT TGG TTG ACC TTT GTA CAT TAA 535This study
    nucSp nuc 61.06V01281 745GAT GGA AAA ATG GTA AAC GAA G766This study
    nucAb nuc 69.12V01281 789AGC CAA GCC TTG ACG AAC TAA AGC766 7
    seaSb sea 64.05M18970 487CCT TTG GAA ACG GTT AAA ACG507 3
    seaSp sea 68.83M18970 531GGA GTT GGA TCT TCA AGC AAG ACG 554 3
    seaAp sea 63.87M18970 613TCT GAA CCT TCC CAT CAA AAA C592 3
    seaAb sea 62.91M18970 691 TTGA ATA CTG TCC TTG AGC ACC670 43
    sebSb seb 64.82M11118 634TCG CAT CAA ACT GAC AAA CG653 3
    sebSp seb 61.1M11118 662 GTAT GTA TGG TGG TGT AAC TGA GC685 43
    sebAp seb 60.06M11118 831 CA CCA AAT AGT GAC GAG TTA GG810 43
    sebAb seb 60.4M11118 924CAT GTC ATA CCA AAA GCT ATT CTC901 3
    secSb sec 62.5X05815 664 G CTC AAG AAC TAG ACA TAA AAG CTA GG690 3
    secSp sec 63.13X05815 772AAC GG(/a)C AAT ACT TTT TGG TAT GAT795 3
    secAp sec 61.4X05815 885 CTT CAC A(/t)CT TTT AGA ATC AAC CG863 43
    secAb sec 60.4X05815 935TCA AAA TCG GAT TAA CAT TAT CC913 3
    sedSb sed 60.2M28521 332CTA GTT TGG TAA TAT CTC CTT TAA ACG358 3
    sedSp sed 64.91M28521 360TAA AGC CAA TGA AAA CAT TGA TTC A384 3
    sedAp sed 60.85M28521 491CTT TTA TTT TCT CCT ATT ATT GG ATTTTT463 30
    sedAb sed 61.9M28521 653 CAA TTA ATG CTA TAT CTT ATA GGG TAA ACA TC622 3
    seeSb see 63.41M21319 424 C GAT TGA CCG AAG AAA AAA AAG445 30
    seeSp see 60.2M21319 479 CTA CAG TAC CTA TAG ATA AAG TTA AAA CAA GC510 3
    seeAp see 66.87M21319 613TTT GCA CCT TAC CGC CAA AG594 3
    seeAb see 60.38M21319 659TAA CTT ACC GTG GAC CCT TC640 3
    segSb seg 66.14AF064773 229CAA CCC/T GAT CCT AAA TTA GAC GAA C253 2
    segSp seg 63.09AF064773 285GGG AAC TAT GGG T(/a)AA TGT AAT GAA TC310 2
    segAp seg 62.61AF064773 338CTT CCT TCA ACA GGT GGA GAC318 2
    segAb seg 62.91AF064773 485/401GGA ACG CCA AAA ATG TCT ACT T464/379 35
    sehSb seh 60.86U11702 407TTA GAA ATC AAG GTG ATA GTG GC 429 2
    sehSp seh 61.25U11702 454ACT GCT GAT TTA GCT CAG AAG TTT A 478 2
    sehAp seh 60.1U11702 575AGT GTT GTA CCT CCA TAT AGA C ATTC550 35
    sehAb seh 60.47U11702 641TTT TGA ATA CCA TCT ACC CAA AC619 2
    seiSb sei 63.01AY158703 396 G GCC ACT TTA TCA GGA CAA TAC TT419 2
    seiSp sei 61.91AY158703 656A CA C(a)TG GTA AAG GC(t)A AAG AAT ATG679 2
    seiAp sei 62.26AY158703 726AAA ACT TAC AGG CAG TCC ATC TC704 2
    seiAb sei 58.23AY158703 818AAT TAT CAT TAG TTA CTA TCT ACA TAT GAT ATT TC784 35
    etaSb eta 61.39M17347 374CTA GTG CAT TTG TTA TTC AAG ACG397 3
    etaSp eta 69.51M17347 414CCA TGC AAA AGC AGA AGT TTC AGC 437 3
    etaAp eta 60.67M17347 492TGC A(/g)TT GAC ACC ATA GTA CTT ATT C468This study
    etaAb eta 62.72M17347 794AAT GCT AAA TCA ACA CCT GC AC773 30
    etbSb etb 61.26M17348 190TAC CAC CTA ATA CCC TAA TAA TCC AA215 3
    etbSp etb 61.37M17348 286GAG ACA GTG CAT TAA ATG AAT AAC TTT312 3
    etbAp etb 62.41M17348 539GAT TTC TTC TGC GCT GTA TTC TT517This study
    etbAb etb 61.16M17348 609 C ATT ATC CGT AAT GTG TGT ATAAA GC584 43
    etdSb etd 61.75AB057421 5963GCT CGG ATA CCC TTA TAA CTT TTC5986This study
    etdSp etd 62.2AB057421 6055CTG AGT CGG GAA ATT CTG G6073 43
    etdAp etd 61.47AB057421 6120CAA CAT GAA TAC CA0A CTA ACT CTC C6096This study
    etdAb etd 61.88AB057421 6259CAT TAC TAA TGA GAC TGT AAT TCA GCT CT6231This study
    tsstSb tsst-1 65.22J02615 348AAG CCA ACA TAC TAG CGA AGG AAC371 3
    tsstSp tsst-1 60.5J02615 394GGC GTT ACA AAT ACT GAA AAA TTA C418 30
    tsstAp tsst-1 64.36J02615 495ATC GAA CTT TGG CCC(/a) ATA CTT T474 3
    tsstAb tsst-1 61.03J02615 556 GTA TTT GAG TTA GCT GAT GAC GAA533 43
    pvlSb pvl 65.29X72700 2651TTT TAG GCT CAA GAC AAA GCA AC2673This study
    pvlAp pvl 65.3X72700 2731TAC CTC TGG ATA ACA CTG GCA TTT T2707 11
    pvlSp pvl 61.76X72700 2733CTT CAA TCC AGA ATT TAT TGG TGT 2756 11
    pvlAb pvl 65.8X72700 2783TTT GCA GCG TTT TGT TTT CG2764 11
    • ↵ a S, sense; A, antisense; b, biotin labeled (all the primers were biotin labeled at the 5′ end); p, probe (all the probes were 5′ end C6 amine labeled).

    • ↵ b T m values were provided by the primer synthesizer (Sigma-Aldrich).

    • ↵ c Boldface numbers represent the numbered base positions at which primer/probe sequences start and finish (starting at point “1” of the corresponding GenBank sequence). Underlined portions indicate modifications of published primer/probe sequences. The bases in parenthesis represent sequences with polymorphisms compared with GenBank sequences or our own sequencing results (for five probes with heterogeneous hybridization).

    • ↵ d Primers and probes were used as previously published (some with modification) except, as indicated, those designed for this study.

  • TABLE 3.

    Primers used for PCR sequencing of nuc, femA, and spa genes

    PrimerTargetTm (°C)GenBank accession no.Primer sequence (5′-3′)c
    nucS1a nuc 60.3V01281 226ATGACAGAATACTTATTAAGTGCTGG251
    nucS2b nuc 60.6V01281 232GAATACTTATTAAGTGCTGGCATATG257
    nucA1b nuc 63.9V01281 908TGACCTGAATCAGCGTTGTC889
    nucA2a nuc 63.7V01281 912TTATTGACCTGAATCAGCGTTG891
    femAS1a femA 64.1X17688 577ATGAAATTAATTAACGAGAGACAAATAGGAG607
    femAS2b femA 65.4X17688 591CGAGAGACAAATAGGAGTAATGATAATGAAG621
    femAA0b femA 67.3X17688 1868CTGTCTTTAACTTTTTTAAGTGCGGTATATGC1837
    femAAa femA 68.3X17688 1878CTAAAAAATTCTGTCTTTAACTTTTTTAAGTGCGG1844
    spaSa spa 71.7J01786 1077CTT CAT CCA AAG CCT TAA AGA CGA TCC TTC1106
    spaAa spa 71.4J01786 1543CAA TTT TGTCAG CAG TAG TGC CGT TTG1517
    spaSEQb spa 71.9J01786 1540TTT TGTCAG CAG TAG TGC CGT TTG CT1515
    • ↵ a For most targets, outer primers were used for amplification and, less commonly, for sequencing.

    • ↵ b Inner primers were mainly used for sequencing, since they gave better results.

    • ↵ c Boldface numbers represent the numbered base positions at which primer sequences start and finish (starting at point “1” of the corresponding GenBank sequence).

  • TABLE 4.

    Comparison of discriminatory powers of each genotyping method and various combinations of methods for 42 MRSA strains using Simpson index of diversity

    Genotyping method(s)No. of types% of largest typeDIa
    Individual
        SCCmec945.20.764
        nuc sequence types738.10.77
        femA sequence types938.10.794
        TGPs1423.80.88
        MLST1523.80.882
        spa types22190.926
    Combinations
        femA-spa-TGP2714.30.959
        TGP-spa2714.30.959
        TGP-spa-nuc2714.30.959
        TGP-spa-SCCmec309.50.98
        femA-spa-TGP-SCCmec319.50.981
        femA-spa-TGP-nuc-MLST-SCCmec349.50.987
    • ↵ a DI, Simpson index, calculated according to the method of Hunter and Gaston (16).

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Comparison of Single- and Multilocus Sequence Typing and Toxin Gene Profiling for Characterization of Methicillin-Resistant Staphylococcus aureus
Yongwei Cai, Fanrong Kong, Qinning Wang, Zhongsheng Tong, Vitali Sintchenko, Xianyu Zeng, Gwendolyn L. Gilbert
Journal of Clinical Microbiology Oct 2007, 45 (10) 3302-3308; DOI: 10.1128/JCM.01082-07

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Comparison of Single- and Multilocus Sequence Typing and Toxin Gene Profiling for Characterization of Methicillin-Resistant Staphylococcus aureus
Yongwei Cai, Fanrong Kong, Qinning Wang, Zhongsheng Tong, Vitali Sintchenko, Xianyu Zeng, Gwendolyn L. Gilbert
Journal of Clinical Microbiology Oct 2007, 45 (10) 3302-3308; DOI: 10.1128/JCM.01082-07
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KEYWORDS

Bacterial Typing Techniques
DNA, Bacterial
methicillin resistance
Sequence Analysis, DNA
Staphylococcus aureus

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