This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kingsley, R. A.
Right arrow Articles by Williams, P. H.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kingsley, R. A.
Right arrow Articles by Williams, P. H.
Agricola
Right arrow Articles by Kingsley, R. A.
Right arrow Articles by Williams, P. H.

 Previous Article  |  Next Article 

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.

Ferrioxamine-Mediated Iron(III) Utilization by Salmonella enterica

Robert A. Kingsley,1,2 Rolf Reissbrodt,3 Wolfgang Rabsch,3 Julian M. Ketley,4 Renée M. Tsolis,5 Paul Everest,6 Gordon Dougan,6 Andreas J. Bäumler,2 Mark Roberts,7 and Peter H. Williams1,*

Department of Microbiology and Immunology, University of Leicester, Leicester LE1 9HN,1 Department of Genetics, University of Leicester, Leicester LE1 7RH,4 Department of Biochemistry, Wolfson Laboratories, Imperial College of Science, Technology and Medicine, London SW7 2AY,6 and Department of Veterinary Pathology, University of Glasgow Veterinary School, Glasgow G61 1QH,7 United Kingdom; Department of Medical Microbiology and Immunology, Texas A&M University, College Station, Texas 77843-11142; Robert Koch Institute, Wernigerode Branch, D-38855 Wernigerode, Germany3; and Department of Veterinary Pathobiology, Texas A&M University, College Station, Texas 77843-44675

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.

* 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.


This article has been cited by other articles:

  • Winter, S. E., Thiennimitr, P., Nuccio, S.-P., Haneda, T., Winter, M. G., Wilson, R. P., Russell, J. M., Henry, T., Tran, Q. T., Lawhon, S. D., Gomez, G., Bevins, C. L., Russmann, H., Monack, D. M., Adams, L. G., Baumler, A. J. (2009). Contribution of Flagellin Pattern Recognition to Intestinal Inflammation during Salmonella enterica Serotype Typhimurium Infection. Infect. Immun. 77: 1904-1916 [Abstract] [Full Text]  
  • Wei, X., Sayavedra-Soto, L. A., Arp, D. J. (2007). Characterization of the ferrioxamine uptake system of Nitrosomonas europaea. Microbiology 153: 3963-3972 [Abstract] [Full Text]  
  • Llamas, M. A., Sparrius, M., Kloet, R., Jimenez, C. R., Vandenbroucke-Grauls, C., Bitter, W. (2006). The Heterologous Siderophores Ferrioxamine B and Ferrichrome Activate Signaling Pathways in Pseudomonas aeruginosa.. J. Bacteriol. 188: 1882-1891 [Abstract] [Full Text]  
  • Yamanaka, K., Oikawa, H., Ogawa, H.-o., Hosono, K., Shinmachi, F., Takano, H., Sakuda, S., Beppu, T., Ueda, K. (2005). Desferrioxamine E produced by Streptomyces griseus stimulates growth and development of Streptomyces tanashiensis. Microbiology 151: 2899-2905 [Abstract] [Full Text]  
  • Reissbrodt, R., Rassbach, A., Burghardt, B., Rienacker, I., Mietke, H., Schleif, J., Tschape, H., Lyte, M., Williams, P. H. (2004). Assessment of a New Selective Chromogenic Bacillus cereus Group Plating Medium and Use of Enterobacterial Autoinducer of Growth for Cultural Identification of Bacillus Species. J. Clin. Microbiol. 42: 3795-3798 [Abstract] [Full Text]  
  • Rabsch, W., Methner, U., Voigt, W., Tschape, H., Reissbrodt, R., Williams, P. H. (2003). Role of Receptor Proteins for Enterobactin and 2,3-Dihydroxybenzoylserine in Virulence of Salmonella enterica. Infect. Immun. 71: 6953-6961 [Abstract] [Full Text]  
  • Kingsley, R. A., Humphries, A. D., Weening, E. H., de Zoete, M. R., Winter, S., Papaconstantinopoulou, A., Dougan, G., Baumler, A. J. (2003). Molecular and Phenotypic Analysis of the CS54 Island of Salmonella enterica Serotype Typhimurium: Identification of Intestinal Colonization and Persistence Determinants. Infect. Immun. 71: 629-640 [Abstract] [Full Text]  
  • Reissbrodt, R., Rienaecker, I., Romanova, J. M., Freestone, P. P. E., Haigh, R. D., Lyte, M., Tschape, H., Williams, P. H. (2002). Resuscitation of Salmonella enterica Serovar Typhimurium and Enterohemorrhagic Escherichia coli from the Viable but Nonculturable State by Heat-Stable Enterobacterial Autoinducer. Appl. Environ. Microbiol. 68: 4788-4794 [Abstract] [Full Text]  
  • Zhang, S., Santos, R. L., Tsolis, R. M., Stender, S., Hardt, W.-D., Baumler, A. J., Adams, L. G. (2002). The Salmonella enterica Serotype Typhimurium Effector Proteins SipA, SopA, SopB, SopD, and SopE2 Act in Concert To Induce Diarrhea in Calves. Infect. Immun. 70: 3843-3855 [Abstract] [Full Text]  
  • Collins, H. L., Kaufmann, S. H. E., Schaible, U. E. (2002). Iron Chelation Via Deferoxamine Exacerbates Experimental Salmonellosis Via Inhibition of the Nicotinamide Adenine Dinucleotide Phosphate Oxidase-Dependent Respiratory Burst. J. Immunol. 168: 3458-3463 [Abstract] [Full Text]  
  • Townsend, S. M., Kramer, N. E., Edwards, R., Baker, S., Hamlin, N., Simmonds, M., Stevens, K., Maloy, S., Parkhill, J., Dougan, G., Baumler, A. J. (2001). Salmonella enterica Serovar Typhi Possesses a Unique Repertoire of Fimbrial Gene Sequences. Infect. Immun. 69: 2894-2901 [Abstract] [Full Text]  
  • Reissbrodt, R., Heier, H., Tschäpe, H., Kingsley, R. A., Williams, P. H. (2000). Resuscitation by Ferrioxamine E of Stressed Salmonella enterica Serovar Typhimurium from Soil and Water Microcosms. Appl. Environ. Microbiol. 66: 4128-4130 [Abstract] [Full Text]  
  • Enard, C., Expert, D. (2000). Characterization of a tonB mutation in Erwinia chrysanthemi 3937: TonBEch is a member of the enterobacterial TonB family. Microbiology 146: 2051-2058 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»