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Applied and Environmental Microbiology, April 1999, p. 1610-1618, Vol. 65, No. 4
Department of Microbiology and Immunology,
Received 24 July 1998/Accepted 21 January 1999
Utilization of ferrioxamines as sole sources of iron distinguishes
Salmonella 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 the
foxA 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 foxA
mutation 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.
0099-2240/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Ferrioxamine-Mediated Iron(III) Utilization by
Salmonella enterica
*
Corresponding author. Mailing address: Department of
Microbiology and Immunology, University of Leicester, University
Road, Leicester LE1 9HN, United Kingdom. Phone: 44 116 252 3436. Fax: 44 116 252 5030. E-mail: phw2{at}le.ac.uk.
Applied and Environmental Microbiology, April 1999, p. 1610-1618, Vol. 65, No. 4
0099-2240/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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