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Biometals

, Volume 19, Issue 2, pp 143–157 | Cite as

Feo – Transport of Ferrous Iron into Bacteria

  • Michaël L. Cartron
  • Sarah Maddocks
  • Paul Gillingham
  • C. Jeremy Craven
  • Simon C. Andrews
Article

Summary

Bacteria commonly utilise a unique type of transporter, called Feo, to specifically acquire the ferrous (Fe2+) form of iron from their environment. Enterobacterial Feo systems are composed of three proteins: FeoA, a small, soluble SH3-domain protein probably located in the cytosol; FeoB, a large protein with a cytosolic N-terminal G-protein domain and a C-terminal integral inner-membrane domain containing two ‘Gate’ motifs which likely functions as the Fe2+ permease; and FeoC, a small protein apparently functioning as an [Fe–S]-dependent transcriptional repressor. We provide a review of the current literature combined with a bioinformatic assessment of bacterial Feo systems showing how they exhibit common features, as well as differences in organisation and composition which probably reflect variations in mechanisms employed and function.

Keywords

G-protein SH3 DtxR MntR Gate motif transport manganese FeoA FeoB FeoC Meo 

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References

  1. Andrews, SC, Robinson, AK, Rodriguez-Quinones, F 2003Bacterial iron homeostasisFEMS Microbiol Rev2721537PubMedCrossRefGoogle Scholar
  2. Boyd, J, Oza, MN, Murphy, JR 1990Molecular cloning and DNA sequence analysis of a diphtheria tox iron-dependent regulatory element (dtxR) from Corynebacterium diphtheriaeProc Natl Acad Sci USA87596872PubMedGoogle Scholar
  3. Boyer, E, Bergevin, I, Malo, D, Gros, P, Cellier, MF 2002Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar TyphimuriumInfect Immun70603242PubMedCrossRefGoogle Scholar
  4. Brown, ED 2005Conserved P-loop GTPases of unknown function in bacteria: an emerging and vital ensemble in bacterial physiologyBiochem Cell Biol83738746PubMedCrossRefGoogle Scholar
  5. Cicchetti, P, Mayer, BJ, Thiel, G, Baltimore, D 1992Identification of a protein that binds to the SH3 region of Abl and is similar to Bcr and GAP-rhoScience257803806PubMedGoogle Scholar
  6. Cowart, RE 2002Reduction of iron by extracellular iron reductases: implications for microbial iron acquisitionArch Biochem Biophys1527381CrossRefGoogle Scholar
  7. D’Aquino, J, Ringe, D 2003Determinants of the Src homology domain 3-like foldJ Bacteriol18540814086PubMedCrossRefGoogle Scholar
  8. Dashper, SG, Butler, CA, Lissel, JP, Paolini, RA, Hoffmann, B, Veith, PD, O’Brien-Simpson, NM, Snelgrove, SL, Tsiros, JT, Reynolds, EC 2005A novel Porphyromonas gingivalis FeoB plays a role in manganese accumulationJ Biol Chem28028095102PubMedCrossRefGoogle Scholar
  9. Dussurget, O, Rodriguez, M, Smith, I 1996An ideR mutant of Mycobacterium smegmatis has derepressed siderophore production and an altered oxidative-stress responseMol Microbiol2253544PubMedCrossRefGoogle Scholar
  10. Ebright, RH 1993Transcription activation at class I CAP-dependent promotersMol Microbiol8797802PubMedGoogle Scholar
  11. Gajiwala, KS, Burley, SK 2000Winged helix proteinsCurr Opin Struct Biol10110116PubMedCrossRefGoogle Scholar
  12. Green, J, Paget, MS 2004Bacterial redox sensorsNat Rev Microbiol295466PubMedCrossRefGoogle Scholar
  13. Hantke, K 1987Ferrous iron transport mutants in Escherichia coli K-12FEMS Microbiol Lett445357Google Scholar
  14. Hantke, K 2003Is the bacterial ferrous iron transporter FeoB a living fossilTrends Microbiol11192195PubMedGoogle Scholar
  15. Hill, PJ, Cockayne, A, Landers, P, Morrissey, JA, Sims, CM, Williams, P 1998SirR, a novel iron-dependent repressor in Staphylococcus epidermidisInfect Immun6641234129PubMedGoogle Scholar
  16. Hirokazu, K, Hagino, N, Grossman, AR, Ogawa, T 2001Genes essential to iron transport in the cycanobacterium Synechocystis sp Strain PCC 6803J Bacteriol18327792784CrossRefGoogle Scholar
  17. Kammler, M, Schon, C, Hantke, K 1993Characterisation of the ferrous iron uptake system of Escherichia coliJ Bacteriol17562126219PubMedGoogle Scholar
  18. Kehres, DG, Janakiraman, A, Hauch, JM, Maguire, ME 2002SitABCD is the alkaline Mn2+ transporter of Salmonella enterica serovar TyphimuriumJ Bacteriol.18431593166PubMedCrossRefGoogle Scholar
  19. Loewen, SK, Ng, AM, Yao, SY, Cass, CE, Baldwin, SA, Young, JD 1999Identification of amino acid residues responsible for the pyrimidine and purine nucleoside specificities of human concentrative Na+ nucleoside cotransporters hCNT1 and hCNT2J Biol Chem2742447524484PubMedCrossRefGoogle Scholar
  20. Louvel, H, Saint Girons, I, Picardeau, M 2005Isolation and characterisation of FecA- and FeoB-mediated iron acquisition systems of the spirochete Leptospira biflexa by random insertional mutagenesisJ Bacterial18732493254CrossRefGoogle Scholar
  21. Marlovits, TC, Haase, W, Herrmann, C, Aller, SG, Unger, VM 2002The membrane protein FeoB contains an intramolecular G protein essential for Fe(II) uptake in bacteriaProc Natl Acad Sci991624316248PubMedCrossRefGoogle Scholar
  22. Mayer, BJ 2001SH3 domains: complexity in moderationJ Cell Science11412531263PubMedGoogle Scholar
  23. Musacchio, A, Gibson, T, Lehto, VP, Saraste, M 1992aSH3 – an abundant protein domain in search of a functionFEBS Lett3075561CrossRefGoogle Scholar
  24. Musacchio, A, Noble, M, Pauptit, R, Wierenga, R, Saraste, M 1992bCrystal structure of a Src-homology 3 (SH3) domainNature359851854CrossRefGoogle Scholar
  25. Musacchio, A, Saraste, M, Wilmanns, M 1994aHigh-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich peptidesNat Struct Biol1546551CrossRefGoogle Scholar
  26. Musacchio, A, Wilmanns, M, Saraste, M 1994bStructure and function of the SH3 domainProg Biophys Mol Biol61283297CrossRefGoogle Scholar
  27. Oguiza, JA, Tao, X, Marcos, AT, Martin, JF, Murphy, JR 1995Molecular cloning, DNA sequence analysis, and characterization of the Corynebacterium diphtheriae DtxR homolog from Brevibacterium lactofermentumJ BacteriolVol465467Google Scholar
  28. Patzer, SI, Hankte, K 2001Dual repression by Fe2+-Fur and Mn2+-MntR of the mntH gene, encoding an NRAMP-like Mn2+ transporter in Escherichia coliJ Bacteriol183480613PubMedCrossRefGoogle Scholar
  29. Pohl, E, Holmes, RK, Hol, WG 1998Motion of the DNA-binding domain with respect to the core of the diphtheria toxin repressor (DtxR) revealed in the crystal structures of apo- and holo-DtxRJ Biol Chem273224207PubMedCrossRefGoogle Scholar
  30. Pohl, E, Holmes, RK, Hol, WG 1999Crystal structure of the iron-dependent regulator (IdeR) from Mycobacterium tuberculosis shows both metal binding sites fully occupiedJ Mol Biol285114556PubMedCrossRefGoogle Scholar
  31. Rensing, C, Ghosh, M, Rosen, BP 1999Families of Soft-Metal-Ion-Transporting ATPasesJ Bacteriol18158915897PubMedGoogle Scholar
  32. Robey, M, Cianciotto, NP 2002Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infectionInfect Immun7056595669PubMedCrossRefGoogle Scholar
  33. Runyen-Janecky, LJ, Reeves, SA, Gonzales, EG, Payne, SM 2003Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cellsInfect Immun71191928PubMedCrossRefGoogle Scholar
  34. Schwartz, M 2005Rho signalling at a glanceJ Cell Science11754475458Google Scholar
  35. Severance, S, Chakraborty, S, Kosman, DJ 2004The Ftr1p iron permease in the yeast plasma membrane: orientation, topology and structure-function relationshipsBiochem J380487496PubMedCrossRefGoogle Scholar
  36. Siderovski, DP, Willard, FS 2005The GAP’s, GEF’s and GDI’s of heterotrimeric G-protein alpha subunitsInt J Biol Sci15166PubMedGoogle Scholar
  37. Sprang, SR 1997G protein mechanisms: insights from structural analysisAnnu Rev Biochem66639678PubMedCrossRefGoogle Scholar
  38. Stojiljkovic, I, Cobeljic, M, Hantke, K 1993Escherichia coli K-12 ferrous iron uptake mutants are impaired in their ability to colonize the mouse intestineFEMS Microbiol Lett1081115PubMedGoogle Scholar
  39. Tao, X, Schiering, N, Zeng, HY, Ringe, D, Murphy, JR 1994Iron, DtxR, and the regulation of diphtheria toxin expressionMol Microbiol14191197PubMedGoogle Scholar
  40. Todd, JD, Wexler, M, Sawers, G, Yeoman, KH, Poole, PS, Johnston, AW 2002RirA, an iron-responsive regulator in the symbiotic bacterium Rhizobium leguminosarumMicrobiology14840594071PubMedGoogle Scholar
  41. Tsolis, RM, Baumler, AJ, Heffron, F, Stojiljkovic, I 1996Contribution of TonB- and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouseInfect Immun6445494556PubMedGoogle Scholar
  42. Velayudhan, J, Hughes, NJ, McColm, AA, Bagshaw, J, Clayton, CL, Andrews, SC, Kelly, DJ 2000Iron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporterMol Microbiol37274286PubMedCrossRefGoogle Scholar
  43. Zaharik, ML, Cullen, VL, Fung, AM, Libby, SL, Kujat Choy, SL, Coburn, B, Kehres, DG, Maguire, ME, Fang, FC, Finlay, BB 2004he Salmonella enterica Serovar Typhimurium divalent cation transport systems MntH and SitABCD are essential for virulence in an Nramp1G169 murine typhoid modelInfect Immun7255225525PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Michaël L. Cartron
    • 1
  • Sarah Maddocks
    • 1
  • Paul Gillingham
    • 2
  • C. Jeremy Craven
    • 2
  • Simon C. Andrews
    • 1
  1. 1.School of Biological Sciences (AMS Building)University of ReadingWhiteknightsUK
  2. 2.Department of Molecular Biology and BiotechnologyUniversity of SheffieldFirth Court, Western BankUK

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