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Genomics and Proteomics

Differences in Gene Content between Salmonella enterica Serovar Enteritidis Isolates and Comparison to Closely Related Serovars Gallinarum and Dublin

S. Porwollik, C. A. Santiviago, P. Cheng, L. Florea, M. McClelland
S. Porwollik
1Sidney Kimmel Cancer Center, 10835 Road to the Cure, San Diego, California 92121
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C. A. Santiviago
1Sidney Kimmel Cancer Center, 10835 Road to the Cure, San Diego, California 92121
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P. Cheng
1Sidney Kimmel Cancer Center, 10835 Road to the Cure, San Diego, California 92121
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L. Florea
2George Washington University, 801 22nd Street NW, Suite 704, Washington, DC 20052, and Center for Food Safety and Applied Nutrition, Food and Drug Administration, 8301 Muirkirk Rd., Laurel, Maryland 20708
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M. McClelland
1Sidney Kimmel Cancer Center, 10835 Road to the Cure, San Diego, California 92121
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  • For correspondence: mmcclelland@skcc.org
DOI: 10.1128/JB.187.18.6545-6555.2005
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  • FIG. 1.
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    FIG. 1.

    Genetic regions of diversity in serovar Enteritidis, Dublin, and Gallinarum isolates compared to serovar Enteritidis PT4. (A) Regions that distinguish serovar Enteritidis isolates. (B) Additional regions of difference detected in serovar Dublin and Gallinarum isolates. (C) Further regions of difference detected in unusual SARB isolates. Presence status is color coded: red, absent; light red, mostly absent; gray, uncertain; light blue, mostly present; blue, present. Strain designations correspond to the numbers in Table 1. Regions are described in detail in Table 2 (panels A and B) and Table S2 in the supplemental material (panel C).

  • FIG. 2.
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    FIG. 2.

    Lineages of serovar Enteritidis strains based on presence of a subset of phage regions. Isolates in this study were grouped based on absence/presence patterns of regions A06 (ST64B-like phage), A19 (Fels-2 regions), and the Typhi CT18 phage regions A22 to A24. Deviation of one character status was allowed. The strains in italics are phage types of the PT4-like lineage, and strains in boldface are PT8-like phage types, according to Guard-Petter (9). Strain numbers correspond to Table 1.

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  • TABLE 1.

    Strains used in this study

    Strain no.Strain nameSerovar/biovarPhage or MLEE typeIsolationbSource
    1MZ 648EnteritidisPT1Denmark, 1985, humanJ. Garaizar
    2MZ 649EnteritidisPT2Denmark, 1987, humanJ. Garaizar
    3MZ 634EnteritidisPT4Spain, 1983, humanJ. Garaizar
    4MZ 636EnteritidisPT4bSpain, 1993, waterJ. Garaizar
    5MZ 637EnteritidisPT5Spain, 1993, foodJ. Garaizar
    6MZ 638EnteritidisPT6aSpain, 1994, waterJ. Garaizar
    7MZ 635EnteritidisPT7aSpain, 1983, humanJ. Garaizar
    8SGSC2377EnteritidisPT8CanadaK. Sanderson
    9MZ 650EnteritidisPT8Denmark, 1983, chickenJ. Garaizar
    1021027EnteritidisPT13aP. Fields
    1121046EnteritidisPT13aP. Fields
    12MZ 655EnteritidisPT23Denmark, 1997, chickenJ. Garaizar
    13MZ 646EnteritidisPT25Denmark, 1996, humanJ. Garaizar
    14MZ 672Enteritidis?Germany, pigeonA. Helm
    15MZ743EnteritidisPT6aUSA, KS, 1948, guinea pigP. Fields
    16MZ744EnteritidisPT13aUSA, 1948, guinea pigP. Fields
    17MZ745EnteritidisPT35USA, GA, 1949P. Fields
    18MZ746EnteritidisPT13aUSA, 1949P. Fields
    19MZ747EnteritidisPT8USA, NJ, 1950P. Fields
    20MZ748EnteritidisPT13aUSA, 1950, mouseP. Fields
    21MZ749EnteritidisPT4bUSA, CA, 1950, ratP. Fields
    22MZ750EnteritidisPT8USA, TX, 1950,P. Fields
    23SARB16EnteritidisEn1, PT13aUSA, Rhode IslandK. Sanderson
    24SARB18EnteritidisEn3, PT4USA, ConnecticutK. Sanderson
    25MZ 647DublinDenmark, 1984, humanJ. Garaizar
    26SARB12DublinDu1USA, Idaho, cattle, 1986K. Sanderson
    27SARB13DublinDu3France, bovine, 1982K. Sanderson
    2899113Gallinarum/PullorumCanada, 1999J. Guard-Bouldin
    2999117Gallinarum/PullorumCanada, 1999J. Guard-Bouldin
    307865LGallinarum/PullorumUSA, 1997J. Frye
    3117368LGallinarum/PullorumUSA, 2003J. Frye
    32SARB51Gallinarum/PullorumPu3GermanyK. Sanderson
    33Sg9Gallinarum/GallinarumT. Wallis
    34SgJ91Gallinarum/GallinarumT. Wallis
    35287/91Gallinarum/GallinarumSequenced isolate, 1991Sanger Center
    36SARB52Gallinarum/PullorumPu4GermanyK. Sanderson
    37SARB17EnteritidisEn2, RDNCaBrazilK. Sanderson
    38SARB20EnteritidisEn7, RDNCSwitzerlandK. Sanderson
    39MZ630EnteritidisPT4sequenced isolateSanger Center
    • ↵ a RDNC, reactive to phages in serovar Enteritidis phage-typing scheme (38) but do not conform to common phage types.

    • ↵ b Location, year, source.

  • TABLE 2.

    Regions differing from the sequenced serovar Enteritidis PT4 isolate in serovar Enteritidis, Dublin, and Gallinarum strainsa

    Region no.aLocation startApprox size (kb)Gene rangecGene and descriptionDiffering strainsd
    EnteritidisDublinGallinarumOther SARB
    Genes present in PT4
        A01b02498061.82428-3538
        A0203096346.7STM0266-02892428-3536,37
        A0312757687.9STM1834-1843 rrmA 3
        A04b146968211.6Phage?15,1725-2728-3536-38
        A0516596343.2STM1489-1491 ynfK 18
        A06b202051538.4ST64B phage?2,8-11,12,15-2428-3536-38
        A0723024172.5STM2200-2201 lysP 18-20
        A08287552412.6STM2844-2858Hydrogenase 3 operon7
        A0929114154.6STM2883-2886 sipBCD, sicA, part of SPI17
        A10436660950.4STM4270-4312 dcu, pmr, nrf, mel operon7
        A11b46087419.4DNA restriction/methylation?136,37
        A12p_000965.4pSLT001-009DNA replication, rck14272936-38
        A13p_0755011.2pSLT012-026 pef fimbriae14,2425-2728-3536-38
        A14p_1948223.3pSLT027-051 spv operon, resolvase, ccd142936-38
        A15_allp_4320016.1pSLT052-055, pSLT068-084 par, sam, SOS inhibition psi, part of tra locus1425-2729,33,3536-38
        A15_subp_525042.0pSLT073-077Part of tra locus10,11,1525-2729,33,3536-38
        B0100937013.7STM0081-008425,26
        B0203535002.4STM0330-0332Transcriptional regulator?3236,37
        B0305931503.7STM0554-0558 yfd glycosyltransferase2636
        B0408661281.5STM0839-0840 ybiV(2) 28,30-3236,38
        B05b089091925.729
        B0610133818.2STM1004-1056 sspH2 28-3537
        B07_all12427097.7STM0910-0907 plus SPT specSimilar to parts of phage Fels-128,30,3137
        B07_sub12492291.2STM0910-0909Similar to parts of phage Fels-125-2728-3137
        B08144796210.8STM1664-1675 Yersinia invC homolog28,30-32
        B09b15202115.6MFS transport?25-2736-38
        B10b15338581.629
        B1115497425.7STM1590-1594 srfA 34
        B1215912916.4STM1558-1560Glycosyl hydrolases27
        B13_a16006558.9STM1544-1555 pqaA 25-2729,33-35
        B13_b15956574.9STM1556-155832
        B1416683782.1STM1481-1483Cation transport32,35
        B15b17202904.729
        B1618737626.6STM1283-1286Chemotaxis?29,33-35
        B17b212862322.029
        B1823310012.8STM2226-2228 yejKL 35
        B1929393554.2STM2912-291530
        B2029479413.3STM2921-2924 rpoS 32
        B21307121012.3STM3022-3033 std fimbriae29,33-35
        B2238980092STM3823-3824 tor system28,30-32
        B23_a46024672.7STM4519-4521 plus SPT spec28-35
        B23_bb46060761.828-3536,37
    Genes absent in PT4
        A1603099243.9STM0271-02722425-2728-3536,38
        A17_a10995654.6STM1006-1009Parts of phage Gifsy-22425-2736
        A17_b11047404.3STM1010-1018Parts of phage Gifsy-22425-27
        A17_c11093053.7STM1019-1024Parts of phage Gifsy-22425-2736
        A17_d11168579.1STM1031-1040Parts of phage Gifsy-22425-2728-3538
        A17_e11260096.7STM1041-1047Parts of phage Gifsy-22425-2728-3536,38
        A1827620641.7STM2616-2618Part of phage Gifsy-124
        A19_a28447147.2STM2695-2702Parts of phage Fels-22,8-12,15-20,22,2325-2736,38
        A19_b28522121.2STM2703-2704Parts of phage Fels-215,17
        A19_c285556618.0STM2707-2730Parts of phage Fels-22,8-12,15-20,22,232530,3136
        A20482856.9pSLT056-067 ssbB 242728,30-35
        A216751625.8pSLT085-110 tra, trb15,17,242728,30-35
        A2227663591.7STY2887-2888Part of serovar Typhi phage ST272,8-12,16-20,22,232528,30,3136,38
        A2335178672.7STY3662-3667 cII, dam, part of serovar Typhi phage ST352,8-12,16,18-20,22,2328,30,3136
        A24352692612.8STY3674-3691 nuc, part of ST352,8-12,15-20,22,2325-2728,30,3136,38
        A2544989094.2STY4632-4636 Dam, part of serovar Typhi phage SopEST1538
        A26269940825.4SPA2602-2625Serovar Paratyphi A phage SPA-32038
        B2403067239.9STM0268-027525-2738
        B25_a031867913.4STM0279-028925-2738
        B25_b03320861.6STM0290-029125-27
        B2628735424.3STM2731-2738Parts of phage Fels-225-27
        B27_all46_0083031.6R001-R04626
        B27_sub46_141847.5R022-R027 fip, tra, stb2634
        B2818830335.2STY2003-2011Restr/modification, hydrolase, start of Typhi phage ST1829,35
        B2919122091.2STY2043-2045Part of ST1826,27
        B3019213041.3STY2060-2061Part of ST1827
        B3127612197.6STY2882-2889Part of ST2728,30,31
        B3235402510.8STY3693-3694Part of ST3528,30,31
        B33440965264.1STY4521-4597SPI7: samB pil topB27
        B34450834721.4STY4648-4666SPI7: vex/tvi27
        B35_a24880617.6SPA2387-2391Part of serovar Paratyphi A phage SPA-132,34
        B35_b249642010.7SPA2393-2394Parts of SPA-125,2632,34
        B35_c251050417.1SPA2401-2431Part of SPA-132,34
    • ↵ a Regions A are different among serovar Enteritidis strains; regions B have been identified in serovar Dublin and Gallinarum strains.

    • ↵ b Regions are not present in sequenced and annotated genomes of serovar Typhimurium LT2, serovar Typhi CT18, serovar Typhi Ty2, or serovar Paratyphi A SARB42; pSLT, serovar Typhimurium LT2 plasmid; R46, transmission plasmid.

    • ↵ c Range of homologous region in STM, STY, or SPA is indicated. STM, S. enterica serovar Typhimurium LT2; STY, S. enterica serovar Typhi CT18; SPA, S. enterica serovar Paratyphi A SARB42.

    • ↵ d Strain numbers are as in Table 1.

Additional Files

  • Figures
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  • HTML Page - index.htslp

    Files in this Data Supplement:

    • Supplemental file 1 - Table S1, Absence/presence prediction for every gene represented by a probe on the Salmonella array in surveyed Salmonella strains; Table S2, Absence/presence predictions for all regions of divergence identified in arrayed S. enterica serovar Enteritidis, Dublin, and Gallinarum isolates; Table S3, Subspecies I signature genes after compilation of data on all subspecies and 24 S. enterica subspecies I serovars.
      Zipped Excel document, 2MB.
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Differences in Gene Content between Salmonella enterica Serovar Enteritidis Isolates and Comparison to Closely Related Serovars Gallinarum and Dublin
S. Porwollik, C. A. Santiviago, P. Cheng, L. Florea, M. McClelland
Journal of Bacteriology Sep 2005, 187 (18) 6545-6555; DOI: 10.1128/JB.187.18.6545-6555.2005

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Differences in Gene Content between Salmonella enterica Serovar Enteritidis Isolates and Comparison to Closely Related Serovars Gallinarum and Dublin
S. Porwollik, C. A. Santiviago, P. Cheng, L. Florea, M. McClelland
Journal of Bacteriology Sep 2005, 187 (18) 6545-6555; DOI: 10.1128/JB.187.18.6545-6555.2005
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KEYWORDS

Bacterial Typing Techniques
DNA, Bacterial
Genome, Bacterial
Salmonella enteritidis

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