• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of iaiPermissionsJournals.ASM.orgJournalIAI ArticleJournal InfoAuthorsReviewers
Infect Immun. Nov 1996; 64(11): 4549–4556.
PMCID: PMC174411

Contribution of TonB- and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse.

Abstract

We examined the role of iron(II) and iron(III) uptake, mediated by FeoB and TonB, respectively, in infection of the mouse by Salmonella typhimurium. The S. typhimurium feoB gene, encoding a homolog of an Escherichia coli cytoplasmic membrane iron(II) permease, was cloned, and a mutant was generated by allelic exchange. In addition, an S. typhimurium tonB mutant was constructed. Together these two mutations inactivate all known iron uptake systems of S. typhimurium. We examined the abilities of these mutants to grow in vitro and in different compartments of the host. Mutants in feoB were outcompeted by the wild type during mixed colonization of the mouse intestine, but the feoB mutation did not attenuate S. typhimurium for oral or intraperitoneal infection of mice. The tonB mutation attenuated S. typhimurium for infection of mice by the intragastric route but not the intraperitoneal route, and the mutant was recovered in lower numbers from the Peyer's patches and mesenteric lymph nodes than the wild type. These results indicate that TonB-mediated iron uptake contributes to colonization of the Peyer's patches and mesenteric lymph nodes but not the liver and spleen of the mouse. The tonB feoB double mutant, given intraperitoneally, was able to infect the liver and spleen at wild-type doses, indicating that additional iron acquisition systems are used during growth at systemic sites of infection.

Full Text

The Full Text of this article is available as a PDF (265K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bäumler AJ, Hantke K. Ferrioxamine uptake in Yersinia enterocolitica: characterization of the receptor protein FoxA. Mol Microbiol. 1992 May;6(10):1309–1321. [PubMed]
  • Bäumler AJ, Tsolis RM, Heffron F. The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer's patches. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):279–283. [PMC free article] [PubMed]
  • Benjamin WH, Jr, Turnbough CL, Jr, Goguen JD, Posey BS, Briles DE. Genetic mapping of novel virulence determinants of Salmonella typhimurium to the region between trpD and supD. Microb Pathog. 1986 Apr;1(2):115–124. [PubMed]
  • Benjamin WH, Jr, Turnbough CL, Jr, Posey BS, Briles DE. The ability of Salmonella typhimurium to produce the siderophore enterobactin is not a virulence factor in mouse typhoid. Infect Immun. 1985 Nov;50(2):392–397. [PMC free article] [PubMed]
  • Buchmeier NA, Lipps CJ, So MY, Heffron F. Recombination-deficient mutants of Salmonella typhimurium are avirulent and sensitive to the oxidative burst of macrophages. Mol Microbiol. 1993 Mar;7(6):933–936. [PubMed]
  • Carter PB, Collins FM. The route of enteric infection in normal mice. J Exp Med. 1974 May 1;139(5):1189–1203. [PMC free article] [PubMed]
  • Crosa JH. Genetics and molecular biology of siderophore-mediated iron transport in bacteria. Microbiol Rev. 1989 Dec;53(4):517–530. [PMC free article] [PubMed]
  • Dunlap NE, Benjamin WH, Jr, McCall RD, Jr, Tilden AB, Briles DE. A 'safe-site' for Salmonella typhimurium is within splenic cells during the early phase of infection in mice. Microb Pathog. 1991 Apr;10(4):297–310. [PubMed]
  • Fields PI, Swanson RV, Haidaris CG, Heffron F. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5189–5193. [PMC free article] [PubMed]
  • Goldberg MB, Boyko SA, Butterton JR, Stoebner JA, Payne SM, Calderwood SB. Characterization of a Vibrio cholerae virulence factor homologous to the family of TonB-dependent proteins. Mol Microbiol. 1992 Aug;6(16):2407–2418. [PubMed]
  • Grant SG, Jessee J, Bloom FR, Hanahan D. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4645–4649. [PMC free article] [PubMed]
  • Gulig PA, Doyle TJ. The Salmonella typhimurium virulence plasmid increases the growth rate of salmonellae in mice. Infect Immun. 1993 Feb;61(2):504–511. [PMC free article] [PubMed]
  • Günter K, Braun V. In vivo evidence for FhuA outer membrane receptor interaction with the TonB inner membrane protein of Escherichia coli. FEBS Lett. 1990 Nov 12;274(1-2):85–88. [PubMed]
  • Hannavy K, Barr GC, Dorman CJ, Adamson J, Mazengera LR, Gallagher MP, Evans JS, Levine BA, Trayer IP, Higgins CF. TonB protein of Salmonella typhimurium. A model for signal transduction between membranes. J Mol Biol. 1990 Dec 20;216(4):897–910. [PubMed]
  • Jarosik GP, Sanders JD, Cope LD, Muller-Eberhard U, Hansen EJ. A functional tonB gene is required for both utilization of heme and virulence expression by Haemophilus influenzae type b. Infect Immun. 1994 Jun;62(6):2470–2477. [PMC free article] [PubMed]
  • Kammler M, Schön C, Hantke K. Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol. 1993 Oct;175(19):6212–6219. [PMC free article] [PubMed]
  • Kinder SA, Badger JL, Bryant GO, Pepe JC, Miller VL. Cloning of the YenI restriction endonuclease and methyltransferase from Yersinia enterocolitica serotype O8 and construction of a transformable R-M+ mutant. Gene. 1993 Dec 22;136(1-2):271–275. [PubMed]
  • Köster W, Braun V. Iron hydroxamate transport of Escherichia coli: nucleotide sequence of the fhuB gene and identification of the protein. Mol Gen Genet. 1986 Sep;204(3):435–442. [PubMed]
  • Leung KY, Finlay BB. Intracellular replication is essential for the virulence of Salmonella typhimurium. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11470–11474. [PMC free article] [PubMed]
  • Luckey M, Pollack JR, Wayne R, Ames BN, Neilands JB. Iron uptake in Salmonella typhimurium: utilization of exogenous siderochromes as iron carriers. J Bacteriol. 1972 Sep;111(3):731–738. [PMC free article] [PubMed]
  • Nnalue NA, Shnyra A, Hultenby K, Lindberg AA. Salmonella choleraesuis and Salmonella typhimurium associated with liver cells after intravenous inoculation of rats are localized mainly in Kupffer cells and multiply intracellularly. Infect Immun. 1992 Jul;60(7):2758–2768. [PMC free article] [PubMed]
  • Ondraczek R, Hobbie S, Braun V. In vitro activation of the Serratia marcescens hemolysin through modification and complementation. J Bacteriol. 1992 Aug;174(15):5086–5094. [PMC free article] [PubMed]
  • Skare JT, Ahmer BM, Seachord CL, Darveau RP, Postle K. Energy transduction between membranes. TonB, a cytoplasmic membrane protein, can be chemically cross-linked in vivo to the outer membrane receptor FepA. J Biol Chem. 1993 Aug 5;268(22):16302–16308. [PubMed]
  • Stojiljkovic I, Bäumler AJ, Heffron F. Ethanolamine utilization in Salmonella typhimurium: nucleotide sequence, protein expression, and mutational analysis of the cchA cchB eutE eutJ eutG eutH gene cluster. J Bacteriol. 1995 Mar;177(5):1357–1366. [PMC free article] [PubMed]
  • Stojiljkovic I, Cobeljic M, Hantke K. Escherichia coli K-12 ferrous iron uptake mutants are impaired in their ability to colonize the mouse intestine. FEMS Microbiol Lett. 1993 Mar 15;108(1):111–115. [PubMed]
  • Stojiljkovic I, Hantke K. Hemin uptake system of Yersinia enterocolitica: similarities with other TonB-dependent systems in gram-negative bacteria. EMBO J. 1992 Dec;11(12):4359–4367. [PMC free article] [PubMed]
  • Tsolis RM, Bäumler AJ, Stojiljkovic I, Heffron F. Fur regulon of Salmonella typhimurium: identification of new iron-regulated genes. J Bacteriol. 1995 Aug;177(16):4628–4637. [PMC free article] [PubMed]
  • Weinberg ED. Iron withholding: a defense against infection and neoplasia. Physiol Rev. 1984 Jan;64(1):65–102. [PubMed]
  • Yancey RJ, Breeding SA, Lankford CE. Enterochelin (enterobactin): virulence factor for Salmonella typhimurium. Infect Immun. 1979 Apr;24(1):174–180. [PMC free article] [PubMed]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...