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MOLECULAR AND CELLULAR PATHOGENESIS

Iron Starvation of Bordetella avium Stimulates Expression of Five Outer Membrane Proteins and Regulates a Gene Involved in Acquiring Iron from Serum

Terry D. Connell, Amy Dickenson, Andrew J. Martone, Kevin T. Militello, Melanie J. Filiatraut, Mark L. Hayman, Joseph Pitula
Terry D. Connell
Center for Microbial Pathogenesis and the Department of Microbiology, School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, New York 14214
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Amy Dickenson
Center for Microbial Pathogenesis and the Department of Microbiology, School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, New York 14214
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Andrew J. Martone
Center for Microbial Pathogenesis and the Department of Microbiology, School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, New York 14214
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Kevin T. Militello
Center for Microbial Pathogenesis and the Department of Microbiology, School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, New York 14214
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Melanie J. Filiatraut
Center for Microbial Pathogenesis and the Department of Microbiology, School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, New York 14214
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Mark L. Hayman
Center for Microbial Pathogenesis and the Department of Microbiology, School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, New York 14214
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Joseph Pitula
Center for Microbial Pathogenesis and the Department of Microbiology, School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, New York 14214
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DOI: 10.1128/IAI.66.8.3597-3605.1998
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    Fig. 1.

    Growth curves demonstrating Fe starvation of 4169. (A) Growth curve of 4169 cultured in Chelex-treated CDM (○) and in Chelex-treated CDM–36 μM FeSO4 (•). (B) Growth curve of 4169 cultured in BHI (■) and in BHI–100 μM EDDA (□). Each point represents the mean culture density of three independent cultures. Error bars represent 1 standard deviation of the mean.

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    Fig. 2.

    Induction of FeRPs by Fe starvation of B. avium. Lanes: 1, molecular mass standards; 2, 4169 in Chelex-treated CDM–36 μM FeSO4; 3, 4169 in Chelex-treated CDM; 4, 4169 in BHI; 5, 4169 in BHI–100 μM EDDA; 6, 838 in BHI; 7, 838 in BHI–100 μM EDDA; 8, 75 in BHI; 9, 75 in BHI–100 μM EDDA. The location of the 84-, 91.5-, 92-, and 95-kDa FeRPs is marked in brackets. The 51-kDa FeRP, which is evident only in lanes 3 and 5, is marked with asterisks. Lanes 2 to 9 each contain 1 μg of total protein. Molecular masses are in kilodaltons. The gel was stained with silver.

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    Fig. 3.

    SDS-PAGE analysis of the OMPs of B. avium4169 and the transposon mutants Pho-6 and Pho-20. Lanes: 1, molecular mass standards; 2, 4169 in BHI; 3, 4169 in BHI-EDDA; 4, Pho-6 in BHI; 5, Pho-6 in BHI-EDDA; 6, Pho-20 in BHI; 7, Pho-20 in BHI-EDDA. Lanes 2 to 7 each contain 1 μg of total protein. Molecular masses are in kilodaltons. The positions of the 95- and 84-kDa FeRPs that are missing in the outer membrane of Pho-20 are denoted by arrows. The gel was stained with silver.

  • Fig. 4.
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    Fig. 4.

    Growth of 4169 and the transposon mutants Pho-6 and Pho-20. ○, 4169 in Chelex-treated CDM; •, 4169 in Chelex-treated CDM–36 μM FeSO4; □, Pho-6 in Chelex-treated CDM; ■, Pho-6 in Chelex-treated CDM–36 μM FeSO4; ◊, Pho-20 in Chelex-treated CDM; ⧫, Pho-20 in Chelex-treated CDM–36 μM FeSO4. Each point represents the mean culture density obtained from three independent cultures. The error bars represent 1 standard deviation of the mean.

  • Fig. 5.
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    Fig. 5.

    Turkey serum as a source of Fe for 4169 and the transposon mutants Pho-6 and Pho-20. Growth conditions: 1, Chelex-treated CDM; 2, Chelex-treated CDM–36 μM FeSO4; 3, Chelex-treated CDM–1.7% turkey serum; 4, Chelex-treated CDM–1.7% turkey serum–50 μM EDDA; 5, Chelex-treated CDM–1.7% turkey serum–50 μM EDDA–50 μM FeSO4; 6, Chelex-treated CDM–1.7% turkey serum–50 μM EDDA–86 μM FeSO4. Each bar represents the mean stationary-phase culture density obtained from three independent cultures. The error bars represent 1 standard deviation of the mean. An asterisk at the top of a bar indicates that the mean OD600 of the mutant strain is significantly different from the mean OD600 of 4169 for the particular growth condition (P ≤ 0.05). P values are noted for each asterisk.

Tables

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  • Table 1.

    Formula for the CDM for growth ofB. aviuma

    StepIngredient or procedureAmt
    Base solutionKH2PO40.5 g
    Sodium glutamate10.72 g
    NaCl2.5 g
    KCl0.2 g
    MgCl2 · 6H2O0.1 g
    Tris1.525 g
    α-Ketoglutamic acid2.0 g
    Sodium pyruvate2.0 g
    CaCl220.0 mg
    Deionized H2OTo 909.0 ml
    Adjust to pH 7.8 with NaOH, autoclave, and store at 4°C
    CDM supplementAscorbic acid0.2 g
    Glutathione, reduced1.0 g
    Deionized H2OTo 100.0 ml
    Store at −20°C
    l-Cystine supplementDeionized H2O3.0 ml
    HCl (11.6 M)1.0 ml
    l-Cystine0.4 g
    Deionized H2OTo 100.0 ml
    Store at −20°C
    l-Proline supplementl-Proline3.0 g
    Deionized H2OTo 200.0 ml
    Autoclave and store at −20°C
    l-Phenylalanine supplementl-Phenylalanine4.0 g
    Deionized H2OTo 400.0 ml
    Autoclave and store at 4°C
    Vitamins p-Aminobenzoic acid10 mg
    Biotin1 mg
    Folic acid10 mg
    Pyridoxyl HCl80 mg
    Riboflavin40 mg
    Thiamine HCl40 mg
    Calcium pantothenate80 mg
    Nicotinamide200 mg
    Deionized H2O800 ml
    Add 2.5 N NaOH until solution clears
    Add deionized H2O to a final volume of 1,000 ml
    Store at −20°C
    Prepare final mediumBase medium909 ml
    l-Cystine stock10 ml
    l-Proline stock16 ml
    CDM supplement10 ml
    l-Phenylalanine stock40 ml
    Vitamins10 ml
    Sterilize by ultrafiltration (0.2-μm pore size)
    • ↵a CDM may be stored for up to 2 weeks at 4°C. Stock solutions may be stored for up to 3 months.

  • Table 2.

    Alkaline phosphatase activities of the TnphoA mutants of B. avium

    StrainFe availability (sp act)aFold inductionb
    Fe repleteFe limited
    41690.018 ± 0.0010.014 ± 0.0010.8
    Pho-60.004 ± 0.0050.129 ± 0.04232.3
    Pho-200.033 ± 0.0210.217 ± 0.0456.6
    • ↵a Values are the results from three replicate cultures of each strain. All values are means ± SD. Specific activities (41) are reported as micromoles of NPP hydrolyzed per minute per OD600 unit by the formulaActivity=[Δ(OD420−OD550)/0.0162]/OD600 ofthestationary­phasecultureFe-replete results are from cells grown in BHI supplemented with 36 μM FeSO4, and Fe-limited results are from cells grown in BHI supplemented with 100 μM EDDA.

    • ↵b Activity during Fe-limited culture/activity during Fe-replete culture.

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Iron Starvation of Bordetella avium Stimulates Expression of Five Outer Membrane Proteins and Regulates a Gene Involved in Acquiring Iron from Serum
Terry D. Connell, Amy Dickenson, Andrew J. Martone, Kevin T. Militello, Melanie J. Filiatraut, Mark L. Hayman, Joseph Pitula
Infection and Immunity Aug 1998, 66 (8) 3597-3605; DOI: 10.1128/IAI.66.8.3597-3605.1998

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Iron Starvation of Bordetella avium Stimulates Expression of Five Outer Membrane Proteins and Regulates a Gene Involved in Acquiring Iron from Serum
Terry D. Connell, Amy Dickenson, Andrew J. Martone, Kevin T. Militello, Melanie J. Filiatraut, Mark L. Hayman, Joseph Pitula
Infection and Immunity Aug 1998, 66 (8) 3597-3605; DOI: 10.1128/IAI.66.8.3597-3605.1998
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KEYWORDS

Bacterial Outer Membrane Proteins
Bordetella
Gene Expression Regulation, Bacterial
Genes, Bacterial
iron

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