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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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ABSTRACT

Utilization of ferrioxamines as sole sources of iron distinguishesSalmonella enterica serotypes Typhimurium and Enteritidis from a number of related species, including Escherichia coli. Ferrioxamine supplements have therefore been used in preenrichment and selection media to increase the bacterial growth rate while selectivity is maintained. We characterized the determinants involved in utilization of ferrioxamines B, E, and G by S. enterica serotype Typhimurium by performing siderophore cross-feeding bioassays. Transport of all three ferric siderophores across the outer membrane was dependent on the FoxA receptor encoded by the Fur-repressible foxA gene. However, only the transport of ferrioxamine G was dependent on the energy-transducing protein TonB, since growth stimulation of a tonB strain by ferrioxamines B and E was observed, albeit at lower efficiencies than in the parental strain. Transport across the inner membrane was dependent on the periplasmic binding protein-dependent ABC transporter complex comprising FhuBCD, as has been reported for other hydroxamate siderophores of enteric bacteria. The distribution of thefoxA gene in the genus Salmonella, as indicated by DNA hybridization studies and correlated with the ability to utilize ferrioxamine E, was restricted to subspecies I, II, and IIIb, and this gene was absent from subspecies IIIa, IV, VI, and VII (formerly subspecies IV) and Salmonella bongori (formerly subspecies V). S. enterica serotype Typhimurium mutants with either a transposon insertion or a defined nonpolar frameshift (+2) mutation in the foxA gene were not able to utilize any of the three ferrioxamines tested. A strain carrying the nonpolar foxAmutation exhibited a significantly reduced ability to colonize rabbit ileal loops compared to the foxA+ parent. In addition, a foxA mutant was markedly attenuated in mice inoculated by either the intragastric or intravenous route. Mice inoculated with the foxA mutant were protected against subsequent challenge by the foxA+ parent strain.

  • Copyright © 1999 American Society for Microbiology
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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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