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PHYSIOLOGY AND BIOTECHNOLOGY

Ferrioxamine-Mediated Iron(III) Utilization bySalmonella enterica

Robert A. Kingsley, Rolf Reissbrodt, Wolfgang Rabsch, Julian M. Ketley, Renée M. Tsolis, Paul Everest, Gordon Dougan, Andreas J. Bäumler, Mark Roberts, Peter H. Williams
Robert A. Kingsley
Department of Microbiology and Immunology, University of Leicester, Leicester LE1 9HN,
Department of Medical Microbiology and Immunology, Texas A&M University, College Station, Texas 77843-1114;
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Rolf Reissbrodt
Robert Koch Institute, Wernigerode Branch, D-38855 Wernigerode, Germany; and
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Wolfgang Rabsch
Robert Koch Institute, Wernigerode Branch, D-38855 Wernigerode, Germany; and
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Julian M. Ketley
Department of Genetics, University of Leicester, Leicester LE1 7RH,
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Renée M. Tsolis
Department of Veterinary Pathobiology, Texas A&M University, College Station, Texas 77843-4467
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Paul Everest
Department of Biochemistry, Wolfson Laboratories, Imperial College of Science, Technology and Medicine, London SW7 2AY, and
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Gordon Dougan
Department of Biochemistry, Wolfson Laboratories, Imperial College of Science, Technology and Medicine, London SW7 2AY, and
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Andreas J. Bäumler
Department of Medical Microbiology and Immunology, Texas A&M University, College Station, Texas 77843-1114;
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Mark Roberts
Department of Veterinary Pathology, University of Glasgow Veterinary School, Glasgow G61 1QH, United Kingdom;
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Peter H. Williams
Department of Microbiology and Immunology, University of Leicester, Leicester LE1 9HN,
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DOI: 10.1128/AEM.65.4.1610-1618.1999
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  • Fig. 1.
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    Fig. 1.

    Construction of a frameshift mutation in thefoxA gene of S. enterica serotype Typhimurium. (A) Comparison of the nucleotide sequences of the wild-type and mutated foxA alleles, as confirmed by sequence analysis. The mutation consists of a 2-bp (AT) insertion (indicated by plus signs) and a BglII restriction enzyme recognition sequence (indicated by boldface type). The mutation was introduced into a cloned subgenic foxA fragment as described in the text by using primers FXM1 and FXM2, which have mismatching base pairs that include the BglII recognition site (B). (C and D) The mutations were confirmed by Southern hybridization analysis in which we used a subgenic foxA fragment as the probe. (C) Analysis ofBglII-digested chromosomal DNA of parental strain TML (lane 1) and the foxA derivative strain RK102 (lane 2). (D) Analysis of parental strain SL1344 (lane 1) and the foxAderivative strain BK102 (lane 2).

  • Fig. 2.
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    Fig. 2.

    Distribution of the foxA gene and the ability to utilize ferrioxamine E as a sole source of iron among subspecies of the genus Salmonella. (A) Neighbor-joining dendrogram showing the relatedness of the various subspecies, based on variation in the combined coding sequences of five housekeeping genes ofSalmonella spp. (8). The arrows indicate probable introduction by horizontal transfer of SPI1 and SPI2 and of thefoxA gene; ΔfoxA indicates possible deletion of the foxA gene in the subspecies VI lineage. Note that Reeves et al. (35) did not differentiate S. enterica subspecies IV into subspecies IV and VII; therefore, the three serotypes tested were random examples of what was originally designated subspecies IV. The hybridization data are the number of strains that exhibited positive hybridization with thefoxA-specific probe/total number of strains tested. The growth promotion data are the number of strains whose growth was promoted by ferrioxamine E (fE) or coprogen (cop) as a sole source of iron/total number of strains tested. (B) Southern blot analyses of chromosomal DNA of representative strains of each subspecies probed with a foxA-specific DNA fragment. For the SARB collection, only the first 25 of the 72 strains listed by Boyd et al. (7) were used, but all other isolates gave similar positive results with the foxA probe. For the representative serotypes of other subspecies, control hybridizations were performed by using a probe derived from the Salmonella fim operon (1) in order to validate negative foxAhybridizations.

  • Fig. 3.
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    Fig. 3.

    Growth of S. enterica serotype Typhimurium strain AR1258 (entB) (A) and its foxAderivative RK809 (B) in tryptone soy broth that was supplemented with 200 μM 2,2′-bipyridyl and ferrioxamine B (●), E (+), or G (□) (at a concentration of 1 μg/ml) or not supplemented (■). Optical densities at 620 nm (OD620) were determined at intervals during incubation with aeration by shaking at 37°C. The data are from a representative experiment; we performed at least five experiments in which similar results were obtained.

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    Fig. 4.

    Comparison of colonization of rabbit ileal loops byS. enterica serovar Typhimurium strain TML with colonization of rabbit ileal loops by derivative strains TML/nr and RK102 (foxA). We performed competitive colonization experiments involving wild-type strain S. enterica TML and either the nalidixic acid-resistant derivative strain TML/nr or the nalidixic acid-resistant foxA mutant strain RK102 by using a total of 10 ileal loops in two rabbits. Approximately 5-cm-long loops were inoculated with 1:1 mixtures containing 107 or 108 cells. After 28 h the proportion of nalidixic acid-resistant coliform bacteria present in the lumen and associated with the gut tissue was determined. The proportion of nalidixic acid-resistant coliform bacteria recovered was expressed as a log10 value (competitive index) and was subjected to a statistical analysis in which the Student t test was used. The asterisks indicate competitive indices significantly different (P > 0.01) from the input ratio (log101 = 0).

Tables

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  • Table 1.

    Bacterial strains and plasmids used in this study

    Strain or plasmidRelevant characteristicsSource or reference
    S. entericaserotype Typhimurium strains
     ATCC 14028Wild typeATCCa
     AR1258ATCC 14028,entB44
     RK804AR1258,tonB18
     RK809AR1258,foxA::pMAPThis study
     enb-7LT2, class II ent mutant33
     WR1024enb-7, fhuB::MudJLaboratory stock
     SL1344hisG4617
     SL1344/nrSL1344, NalrThis study
     BK102SL1344/nr, foxAThis study
     TMLWild type12
     TML/nrTML, NalrThis study
     RK102TML/nr,foxAThis study
    E. coliSM10λpirF−thi-1 thr-1 leuB6 supE44 tonA21 lacY1 recA::RP4-2-tc::Mu KmrR. Haigh
    Plasmids
     pUC18ColE1,blaLaboratory stock
     pRA17pUC18 carrying the 287-bp foxA fragmentThis study
     pRA5pUC18 carrying the foxA 5′ regionThis study
     pBluescriptSKColE1, blaLaboratory stock
     pRA19pBluescriptSK carrying the mutated 287-bpfoxA fragmentThis study
     pRDH10sacRB cat oriR6K mobRP4, TetrR. Haigh
     pRA21pRDH10 carrying the 287-bp foxAfragmentThis study
     pIRS618pSUKS1 carrying the serovar Typhimurium tonB gene45
     pMAPbla oriR6KmobRP444
    • ↵a ATCC, American Type Culture Collection.

  • Table 2.

    Siderophore cross-feeding of various serotype Typhimurium strainsa

    MediumConcn of 2,2′-bipyridyl (μM)StrainRelevant genotypeResults with the following siderophores:
    Ferrioxamine BFerrioxamine EFerrioxamine GCoprogenEnterobactin
    Vogel-Bonnerb200AR1258entB2829262830
    RK804entB tonB1314555
    RK804(pIRS618)entB tonB+2625232830
    WR1024ent fhuB555530
    RK809entB foxA8552830
    EWMc400SL1344/nrWild type++++ND
    BK102foxA(+)−−+ND
    TML/nrWild type++++ND
    RK102foxA(+)−−+ND
    • ↵a Approximately 106 cells of each strain tested were spread over the surface of Vogel-Bonner or EWM agar. Sterile filter paper discs (diameter, 5 mm), each impregnated with 1 μg of a siderophore, were placed on the agar surfaces.

    • ↵b For the Vogel-Bonner medium bioassays, the sizes (in millimeters) of growth zones around siderophore discs were recorded after 18 h of incubation at 37°C; a value of 5 mm indicates that there was no growth stimulation.

    • ↵c In the EWM bioassays, growth was too diffuse to measure accurately as discrete zones, and so the results were recorded as follows: +, obvious growth; (+), limited growth around the disc; and −, no observable growth after 3 to 4 h of incubation at 37°C. ND, growth stimulation not determined.

  • Table 3.

    Protection of mice previously inoculated with strain BK102 against subsequent challenge with S. enterica serotype Typhimurium strain SL1344/nr

    BK102 inoculum (CFU)aNo. of survivors/no. of mice testedb
    1093/4
    1083/4
    1074/4
    1063/4
    1050/5
    1042/5
    1030/5
    • ↵a The BK102 inoculum was administered 28 days prior to challenge with strain SL1344/nr.

    • ↵b Number of mice surviving 10 days after inoculation with 5 × 108 CFU of SL1344/nr/number of mice tested.

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Ferrioxamine-Mediated Iron(III) Utilization bySalmonella enterica
Robert A. Kingsley, Rolf Reissbrodt, Wolfgang Rabsch, Julian M. Ketley, Renée M. Tsolis, Paul Everest, Gordon Dougan, Andreas J. Bäumler, Mark Roberts, Peter H. Williams
Applied and Environmental Microbiology Apr 1999, 65 (4) 1610-1618; DOI: 10.1128/AEM.65.4.1610-1618.1999

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Ferrioxamine-Mediated Iron(III) Utilization bySalmonella enterica
Robert A. Kingsley, Rolf Reissbrodt, Wolfgang Rabsch, Julian M. Ketley, Renée M. Tsolis, Paul Everest, Gordon Dougan, Andreas J. Bäumler, Mark Roberts, Peter H. Williams
Applied and Environmental Microbiology Apr 1999, 65 (4) 1610-1618; DOI: 10.1128/AEM.65.4.1610-1618.1999
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KEYWORDS

Escherichia coli Proteins
Ferric Compounds
Receptors, Cell Surface
Salmonella Typhimurium
siderophores

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