Skip to main content
SpringerLink
Log in

Feo – Transport of Ferrous Iron into Bacteria

  • Published:
Biometals Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • SC Andrews AK Robinson F Rodriguez-Quinones (2003) ArticleTitleBacterial iron homeostasis FEMS Microbiol Rev 27 215–37 Occurrence Handle12829269 Occurrence Handle1:CAS:528:DC%2BD3sXksVOlt70%3D Occurrence Handle10.1016/S0168-6445(03)00055-X

    Article  PubMed  CAS  Google Scholar 

  • J Boyd MN Oza JR Murphy (1990) ArticleTitleMolecular cloning and DNA sequence analysis of a diphtheria tox iron-dependent regulatory element (dtxR) from Corynebacterium diphtheriae Proc Natl Acad Sci USA 87 5968–72 Occurrence Handle2116013 Occurrence Handle1:CAS:528:DyaK3MXhtlai

    PubMed  CAS  Google Scholar 

  • E Boyer I Bergevin D Malo P Gros MF Cellier (2002) ArticleTitleAcquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium Infect Immun 70 6032–42 Occurrence Handle12379679 Occurrence Handle1:CAS:528:DC%2BD38XotFGks7k%3D Occurrence Handle10.1128/IAI.70.11.6032-6042.2002

    Article  PubMed  CAS  Google Scholar 

  • ED Brown (2005) ArticleTitleConserved P-loop GTPases of unknown function in bacteria: an emerging and vital ensemble in bacterial physiology Biochem Cell Biol 83 738–746 Occurrence Handle16333325 Occurrence Handle1:CAS:528:DC%2BD28XptlKhsg%3D%3D Occurrence Handle10.1139/o05-162

    Article  PubMed  CAS  Google Scholar 

  • P Cicchetti BJ Mayer G Thiel D Baltimore (1992) ArticleTitleIdentification of a protein that binds to the SH3 region of Abl and is similar to Bcr and GAP-rho Science 257 803–806 Occurrence Handle1379745 Occurrence Handle1:CAS:528:DyaK3sXktVegsbk%3D

    PubMed  CAS  Google Scholar 

  • RE Cowart (2002) ArticleTitleReduction of iron by extracellular iron reductases: implications for microbial iron acquisition Arch Biochem Biophys 15 273–81 Occurrence Handle10.1016/S0003-9861(02)00012-7

    Article  Google Scholar 

  • J D’Aquino D Ringe (2003) ArticleTitleDeterminants of the Src homology domain 3-like fold J Bacteriol 185 4081–4086 Occurrence Handle12837782 Occurrence Handle1:CAS:528:DC%2BD3sXlsFahsLg%3D Occurrence Handle10.1128/JB.185.14.4081-4086.2003

    Article  PubMed  CAS  Google Scholar 

  • SG Dashper CA Butler JP Lissel RA Paolini B Hoffmann PD Veith NM O’Brien-Simpson SL Snelgrove JT Tsiros EC Reynolds (2005) ArticleTitleA novel Porphyromonas gingivalis FeoB plays a role in manganese accumulation J Biol Chem 280 28095–102 Occurrence Handle15901729 Occurrence Handle1:CAS:528:DC%2BD2MXmsV2jsrg%3D Occurrence Handle10.1074/jbc.M503896200

    Article  PubMed  CAS  Google Scholar 

  • O Dussurget M Rodriguez I Smith (1996) ArticleTitleAn ideR mutant of Mycobacterium smegmatis has derepressed siderophore production and an altered oxidative-stress response Mol Microbiol 22 535–44 Occurrence Handle8939436 Occurrence Handle1:CAS:528:DyaK28XmvVygtb4%3D Occurrence Handle10.1046/j.1365-2958.1996.1461511.x

    Article  PubMed  CAS  Google Scholar 

  • RH Ebright (1993) ArticleTitleTranscription activation at class I CAP-dependent promoters Mol Microbiol 8 797–802 Occurrence Handle8394979 Occurrence Handle1:CAS:528:DyaK3sXltV2qsL4%3D

    PubMed  CAS  Google Scholar 

  • KS Gajiwala SK Burley (2000) ArticleTitleWinged helix proteins Curr Opin Struct Biol 10 110–116 Occurrence Handle10679470 Occurrence Handle1:CAS:528:DC%2BD3cXhs1Slt7g%3D Occurrence Handle10.1016/S0959-440X(99)00057-3

    Article  PubMed  CAS  Google Scholar 

  • J Green MS Paget (2004) ArticleTitleBacterial redox sensors Nat Rev Microbiol 2 954–66 Occurrence Handle15550941 Occurrence Handle1:CAS:528:DC%2BD2cXpvFWrs74%3D Occurrence Handle10.1038/nrmicro1022

    Article  PubMed  CAS  Google Scholar 

  • K Hantke (1987) ArticleTitleFerrous iron transport mutants in Escherichia coli K-12 FEMS Microbiol Lett 44 53–57 Occurrence Handle1:CAS:528:DyaL2sXlslahs7s%3D

    CAS  Google Scholar 

  • K Hantke (2003) ArticleTitleIs the bacterial ferrous iron transporter FeoB a living fossil Trends Microbiol 11 192–195 Occurrence Handle12781516 Occurrence Handle1:CAS:528:DC%2BD3sXktFGhtb0%3D

    PubMed  CAS  Google Scholar 

  • PJ Hill A Cockayne P Landers JA Morrissey CM Sims P Williams (1998) ArticleTitleSirR, a novel iron-dependent repressor in Staphylococcus epidermidis Infect Immun 66 4123–4129 Occurrence Handle9712757 Occurrence Handle1:CAS:528:DyaK1cXlslCku7o%3D

    PubMed  CAS  Google Scholar 

  • K Hirokazu N Hagino AR Grossman T Ogawa (2001) ArticleTitleGenes essential to iron transport in the cycanobacterium Synechocystis sp Strain PCC 6803 J Bacteriol 183 2779–2784 Occurrence Handle10.1128/JB.183.9.2779-2784.2001

    Article  Google Scholar 

  • M Kammler C Schon K Hantke (1993) ArticleTitleCharacterisation of the ferrous iron uptake system of Escherichia coli J Bacteriol 175 6212–6219 Occurrence Handle8407793 Occurrence Handle1:CAS:528:DyaK2cXkvFOruw%3D%3D

    PubMed  CAS  Google Scholar 

  • DG Kehres A Janakiraman JM Hauch ME Maguire (2002) ArticleTitleSitABCD is the alkaline Mn2+ transporter of Salmonella enterica serovar Typhimurium J Bacteriol. 184 3159–3166 Occurrence Handle12029031 Occurrence Handle1:CAS:528:DC%2BD38XksV2htro%3D Occurrence Handle10.1128/JB.184.12.3159-3166.2002

    Article  PubMed  CAS  Google Scholar 

  • SK Loewen AM Ng SY Yao CE Cass SA Baldwin JD Young (1999) ArticleTitleIdentification of amino acid residues responsible for the pyrimidine and purine nucleoside specificities of human concentrative Na+ nucleoside cotransporters hCNT1 and hCNT2 J Biol Chem 274 24475–24484 Occurrence Handle10455109 Occurrence Handle1:CAS:528:DyaK1MXls1ynsL4%3D Occurrence Handle10.1074/jbc.274.35.24475

    Article  PubMed  CAS  Google Scholar 

  • H Louvel I Saint Girons M Picardeau (2005) ArticleTitleIsolation and characterisation of FecA- and FeoB-mediated iron acquisition systems of the spirochete Leptospira biflexa by random insertional mutagenesis J Bacterial 187 3249–3254 Occurrence Handle1:CAS:528:DC%2BD2MXjvVGqtbY%3D Occurrence Handle10.1128/JB.187.9.3249-3254.2005

    Article  CAS  Google Scholar 

  • TC Marlovits W Haase C Herrmann SG Aller VM Unger (2002) ArticleTitleThe membrane protein FeoB contains an intramolecular G protein essential for Fe(II) uptake in bacteria Proc Natl Acad Sci 99 16243–16248 Occurrence Handle12446835 Occurrence Handle1:CAS:528:DC%2BD38Xps1entr4%3D Occurrence Handle10.1073/pnas.242338299

    Article  PubMed  CAS  Google Scholar 

  • BJ Mayer (2001) ArticleTitleSH3 domains: complexity in moderation J Cell Science 114 1253–1263 Occurrence Handle11256992 Occurrence Handle1:CAS:528:DC%2BD3MXjt1Omt7k%3D

    PubMed  CAS  Google Scholar 

  • A Musacchio T Gibson VP Lehto M Saraste (1992a) ArticleTitleSH3 – an abundant protein domain in search of a function FEBS Lett 307 55–61 Occurrence Handle1:CAS:528:DyaK38Xlt1Kmt7k%3D Occurrence Handle10.1016/0014-5793(92)80901-R

    Article  CAS  Google Scholar 

  • A Musacchio M Noble R Pauptit R Wierenga M Saraste (1992b) ArticleTitleCrystal structure of a Src-homology 3 (SH3) domain Nature 359 851–854 Occurrence Handle1:CAS:528:DyaK38XmsVOgu7w%3D Occurrence Handle10.1038/359851a0

    Article  CAS  Google Scholar 

  • A Musacchio M Saraste M Wilmanns (1994a) ArticleTitleHigh-resolution crystal structures of tyrosine kinase SH3 domains complexed with proline-rich peptides Nat Struct Biol 1 546–551 Occurrence Handle1:CAS:528:DyaK2MXitVGhsLw%3D Occurrence Handle10.1038/nsb0894-546

    Article  CAS  Google Scholar 

  • A Musacchio M Wilmanns M Saraste (1994b) ArticleTitleStructure and function of the SH3 domain Prog Biophys Mol Biol 61 283–297 Occurrence Handle1:CAS:528:DyaK2MXjtF2rsA%3D%3D Occurrence Handle10.1016/0079-6107(94)90003-5

    Article  CAS  Google Scholar 

  • JA Oguiza X Tao AT Marcos JF Martin JR Murphy (1995) ArticleTitleMolecular cloning, DNA sequence analysis, and characterization of the Corynebacterium diphtheriae DtxR homolog from Brevibacterium lactofermentum J Bacteriol Vol 465–467

    Google Scholar 

  • SI Patzer K Hankte (2001) ArticleTitleDual repression by Fe2+-Fur and Mn2+-MntR of the mntH gene, encoding an NRAMP-like Mn2+ transporter in Escherichia coli J Bacteriol 183 4806–13 Occurrence Handle11466284 Occurrence Handle1:CAS:528:DC%2BD3MXlslKkt7o%3D Occurrence Handle10.1128/JB.183.16.4806-4813.2001

    Article  PubMed  CAS  Google Scholar 

  • E Pohl RK Holmes WG Hol (1998) ArticleTitleMotion 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-DtxR J Biol Chem 273 22420–7 Occurrence Handle9712865 Occurrence Handle1:CAS:528:DyaK1cXlvValtrc%3D Occurrence Handle10.1074/jbc.273.35.22420

    Article  PubMed  CAS  Google Scholar 

  • E Pohl RK Holmes WG Hol (1999) ArticleTitleCrystal structure of the iron-dependent regulator (IdeR) from Mycobacterium tuberculosis shows both metal binding sites fully occupied J Mol Biol 285 1145–56 Occurrence Handle9887269 Occurrence Handle1:CAS:528:DyaK1MXhtVGjsLc%3D Occurrence Handle10.1006/jmbi.1998.2339

    Article  PubMed  CAS  Google Scholar 

  • C Rensing M Ghosh BP Rosen (1999) ArticleTitleFamilies of Soft-Metal-Ion-Transporting ATPases J Bacteriol 181 5891–5897 Occurrence Handle10498699 Occurrence Handle1:CAS:528:DyaK1MXmsVOrtrs%3D

    PubMed  CAS  Google Scholar 

  • M Robey NP Cianciotto (2002) ArticleTitleLegionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection Infect Immun 70 5659–5669 Occurrence Handle12228295 Occurrence Handle1:CAS:528:DC%2BD38XnsV2lsbs%3D Occurrence Handle10.1128/IAI.70.10.5659-5669.2002

    Article  PubMed  CAS  Google Scholar 

  • LJ Runyen-Janecky SA Reeves EG Gonzales SM Payne (2003) ArticleTitleContribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells Infect Immun 71 1919–28 Occurrence Handle12654809 Occurrence Handle1:CAS:528:DC%2BD3sXislOhsLk%3D Occurrence Handle10.1128/IAI.71.4.1919-1928.2003

    Article  PubMed  CAS  Google Scholar 

  • M Schwartz (2005) ArticleTitleRho signalling at a glance J Cell Science 117 5447–5458

    Google Scholar 

  • S Severance S Chakraborty DJ Kosman (2004) ArticleTitleThe Ftr1p iron permease in the yeast plasma membrane: orientation, topology and structure-function relationships Biochem J 380 487–496 Occurrence Handle14992688 Occurrence Handle1:CAS:528:DC%2BD2cXksFyhsrw%3D Occurrence Handle10.1042/BJ20031921

    Article  PubMed  CAS  Google Scholar 

  • DP Siderovski FS Willard (2005) ArticleTitleThe GAP’s, GEF’s and GDI’s of heterotrimeric G-protein alpha subunits Int J Biol Sci 1 51–66 Occurrence Handle15951850 Occurrence Handle1:CAS:528:DC%2BD2MXjs1eltb4%3D

    PubMed  CAS  Google Scholar 

  • SR Sprang (1997) ArticleTitleG protein mechanisms: insights from structural analysis Annu Rev Biochem 66 639–678 Occurrence Handle9242920 Occurrence Handle1:CAS:528:DyaK2sXktFOmu7w%3D Occurrence Handle10.1146/annurev.biochem.66.1.639

    Article  PubMed  CAS  Google Scholar 

  • I Stojiljkovic M Cobeljic K Hantke (1993) ArticleTitleEscherichia coli K-12 ferrous iron uptake mutants are impaired in their ability to colonize the mouse intestine FEMS Microbiol Lett 108 111–5 Occurrence Handle8472918 Occurrence Handle1:CAS:528:DyaK3sXitV2gtrY%3D

    PubMed  CAS  Google Scholar 

  • X Tao N Schiering HY Zeng D Ringe JR Murphy (1994) ArticleTitleIron, DtxR, and the regulation of diphtheria toxin expression Mol Microbiol 14 191–197 Occurrence Handle7830565 Occurrence Handle1:CAS:528:DyaK2MXhslehsbk%3D

    PubMed  CAS  Google Scholar 

  • JD Todd M Wexler G Sawers KH Yeoman PS Poole AW Johnston (2002) ArticleTitleRirA, an iron-responsive regulator in the symbiotic bacterium Rhizobium leguminosarum Microbiology 148 4059–4071 Occurrence Handle12480909 Occurrence Handle1:CAS:528:DC%2BD3sXivVSktrw%3D

    PubMed  CAS  Google Scholar 

  • RM Tsolis AJ Baumler F Heffron I Stojiljkovic (1996) ArticleTitleContribution of TonB- and Feo-mediated iron uptake to growth of Salmonella typhimurium in the mouse Infect Immun 64 4549–4556 Occurrence Handle8890205 Occurrence Handle1:CAS:528:DyaK28XmsVWntrY%3D

    PubMed  CAS  Google Scholar 

  • J Velayudhan NJ Hughes AA McColm J Bagshaw CL Clayton SC Andrews DJ Kelly (2000) ArticleTitleIron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporter Mol Microbiol 37 274–286 Occurrence Handle10931324 Occurrence Handle1:CAS:528:DC%2BD3cXls12ktL8%3D Occurrence Handle10.1046/j.1365-2958.2000.01987.x

    Article  PubMed  CAS  Google Scholar 

  • ML Zaharik VL Cullen AM Fung SL Libby SL Kujat Choy B Coburn DG Kehres ME Maguire FC Fang BB Finlay (2004) ArticleTitlehe Salmonella enterica Serovar Typhimurium divalent cation transport systems MntH and SitABCD are essential for virulence in an Nramp1G169 murine typhoid model Infect Immun 72 5522–5525 Occurrence Handle15322058 Occurrence Handle1:CAS:528:DC%2BD2cXnt1Cht70%3D Occurrence Handle10.1128/IAI.72.9.5522-5525.2004

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Biological Sciences (AMS Building), University of Reading, Whiteknights, Reading, RG6 6AJ, UK

    Michaël L. Cartron, Sarah Maddocks & Simon C. Andrews

  2. Department of Molecular Biology and Biotechnology, University of Sheffield, Firth Court, Western Bank, Sheffield, S10 2TN, UK

    Paul Gillingham & C. Jeremy Craven

Authors
  1. Michaël L. Cartron
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah Maddocks
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul Gillingham
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Jeremy Craven
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Simon C. Andrews
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Simon C. Andrews.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cartron, M.L., Maddocks, S., Gillingham, P. et al. Feo – Transport of Ferrous Iron into Bacteria. Biometals 19, 143–157 (2006). https://doi.org/10.1007/s10534-006-0003-2

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-006-0003-2

Keywords

Search

Navigation