Skip to main content

Acquisition of Iron by Bacteria

Part of the Microbiology Monographs book series (MICROMONO,volume 6)

Abstract

Bacteria have evolved multiple mechanisms to cope with the extreme iron limitations in their natural environments. Fe3+ forms insoluble hydroxy aquo complexes. The free Fe3+ concentration lies orders of magnitude below the concentration required for microbial growth (0.1 μM). Bacteria synthesize and secrete low-molecular-weight compounds, called siderophores, which bind Fe3+ with very high affinity and specificity, and host organisms of bacteria bind Fe3+ to proteins that serve as iron sources for bacteria. Energy-coupled transport systems bring Fe3+, Fe3+-siderophores, and heme across the outer membrane, the periplasm, and the cytoplasmic membrane into the bacterial cytoplasm. There, iron is released from the carrier molecules and incorporated mostly into heme and iron-sulfur proteins. Intracellular iron metabolism is poorly understood. The transport systems and the biosynthesis of the siderophores are regulated by proteins, usually by Fur in Gram-negative bacteria, and DtxR and IdeR in Gram-positive bacteria. These proteins act as transcriptional repressors when loaded with Fe2+. Additional regulatory devices control siderophore biosynthesis and transport. The Fec-type of regulation is of particular interest because it involves a novel mechanism in which the ferric siderophore binds to the outer membrane transport protein and from there induces transcription of the transport and biosynthesis genes in the cytoplasm. Another recently detected device is the regulation of genes positively regulated by Fur via RhyB, a small regulatory RNA. RhyB facilitates degradation of positively regulated mRNAs, which does not occur when Fe2+-Fur represses RhyB synthesis.

Keywords

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (Canada)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (Canada)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.00
Price excludes VAT (Canada)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (Canada)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Afonyushkin T, Vecerek B, Moll I, Blasi U, Kaberdin VR (2005) Both RNase E and RNase III control the stability of sodB mRNA upon translational inhibition by the small regulatory RNA RyhB. Nucleic Acids Res 33:1678–1689

    PubMed  CAS  Google Scholar 

  2. Anderson DS, Adhikari P, Nowalk AJ, Chen CY, Mietzner TA (2004) The hFbpABC transporter from Haemophilus influenzae functions as a binding-protein-dependent ABC transporter with high specificity and affinity for ferric iron. J Bacteriol 186:6220–6229

    PubMed  CAS  Google Scholar 

  3. Andrews SC, Robinson AK, Rodriguez-Quinones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237

    PubMed  CAS  Google Scholar 

  4. Angerer A, Braun V (1998) Iron regulates transcription of the Escherichia coli ferric citrate transport genes directly and through the transcription initiation proteins. Arch Microbiol 169:483–490

    PubMed  CAS  Google Scholar 

  5. Angerer A, Enz S, Ochs M, Braun V (1995) Transcriptional regulation of ferric citrate transport in Escherichia coli K-12. Fecl belongs to a new subfamily of sigma 70-type factors that respond to extracytoplasmic stimuli. Mol Microbiol 18:163–174

    PubMed  CAS  Google Scholar 

  6. Angerer A, Gaisser S, Braun V (1990) Nucleotide sequences of the sfuA, sfuB, and sfuC genes of Serratia marcescens suggest a periplasmic-binding-protein-dependent iron transport mechanism. J Bacteriol 172:572–578

    PubMed  CAS  Google Scholar 

  7. Baichoo N, Helmann JD (2002) Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J Bacteriol 184:5826–5832

    PubMed  CAS  Google Scholar 

  8. Bearden SW, Perry RD (1999) The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol Microbiol 32:403–414

    PubMed  CAS  Google Scholar 

  9. Beare PA, For RJ, Martin LW, Lamont IL (2003) Siderophore-mediated cell signalling in Pseudomonas aeruginosa: divergent pathways regulate virulence factor production and siderophore receptor synthesis. Mol Microbiol 47:195–207

    PubMed  CAS  Google Scholar 

  10. Beaumont FC, Kang HY, Brickman TJ, Armstrong SK (1998) Identification and characterization of alcR, a gene encoding an AraC-like regulator of alcaligin siderophore biosynthesis and transport in Bordetella pertussis and Bordetella bronchiseptica. J Bacteriol 180:862–870

    PubMed  CAS  Google Scholar 

  11. Bister B, Bischoff D, Nicholson GJ, Valdebenito M, Schneider K, Winkelmann G, Hantke K, Süssmuth RD (2004) The structure of salmochelins: C-glucosylated enterobactins of Salmonella enterica. Biometals 17:471–481

    PubMed  CAS  Google Scholar 

  12. Boonjakuakul JK, Canfield DR, Solnick JV (2005) Comparison of Helicobacter pylori virulence gene expression in vitro and in the Rhesus macaque. Infect Immun 73:4895–4904

    PubMed  CAS  Google Scholar 

  13. Borths EL, Locher KP, Lee AT, Rees DC (2002) The structure of Escherichia coli BtuF and binding to its cognate ATP binding cassette transporter. Proc Natl Acad Sci USA 99:16642–16647

    PubMed  CAS  Google Scholar 

  14. Boyd J, Oza MN, Murphy JR (1990) Molecular cloning and DNA sequence analysis of a diphtheria tox iron-dependent regulatory element (dtxR) from Corynebacterium diphtheriae. Proc Natl Acad Sci USA 87:5968–5972

    PubMed  CAS  Google Scholar 

  15. Boyer E, Bergevin I, Malo D, Gros P, Cellier MF (2002) Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium. Infect Immun 70:6032–6042

    PubMed  CAS  Google Scholar 

  16. Braun M, Endriss F, Killmann H, Braun V (2003) In vivo reconstitution of the FhuA transport protein of Escherichia coli K-12. J Bacteriol 185:5508–5518

    PubMed  CAS  Google Scholar 

  17. Braun V, Hantke K, Köster W (1998) Bacterial iron transport: mechanisms, genetics, and regulation. Met Ions Biol Syst 35:67–145

    PubMed  CAS  Google Scholar 

  18. Braun V, Mahren S (2005) Transmembrane transcriptional control (surface signalling) of the Escherichia coli Fec type. FEMS Microbiol Rev 29:673–684

    PubMed  CAS  Google Scholar 

  19. Breidenstein E, Mahren S, Braun V (2006) Residues involved in FecR binding are localized on one side of the FecA signaling domain in Escherichia coli. J Bacteriol 188:6440–6442

    PubMed  CAS  Google Scholar 

  20. Bruns CM, Nowalk AJ, Arvai AS, McTigue MA, Vaughan KG, Mietzner TA, McRee DE (1997) Structure of Haemophilus influenzae Fe(+3)-binding protein reveals convergent evolution within a superfamily. Nat Struct Biol 4:919–924

    PubMed  CAS  Google Scholar 

  21. Buchanan SK, Smith BS, Venkatramani L, Xia D, Esser L, Palnitkar M, Chakraborty R, van der HD, Deisenhofer J (1999) Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat Struct Biol 6:56–63

    PubMed  CAS  Google Scholar 

  22. Cartron ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC (2006) Feo – transport of ferrous iron into bacteria. Biometals 19:143–157

    PubMed  CAS  Google Scholar 

  23. Chimento DP, Kadner RJ, Wiener MC (2003) The Escherichia coli outer membrane cobalamin transporter BtuB: structural analysis of calcium and substrate binding, and identification of orthologous transporters by sequence/structure conservation. J Mol Biol 332:999–1014

    PubMed  CAS  Google Scholar 

  24. Clancy A, Loar JW, Speziali CD, Oberg M, Heinrichs DE, Rubens CE (2006) Evidence for siderophore-dependent iron acquisition in group B Streptococcus. Mol Microbiol 59:707–721

    PubMed  CAS  Google Scholar 

  25. Clarke TE, Rohrbach MR, Tari LW, Vogel HJ, Koster W (2002) Ferric hydroxamate binding protein FhuD from Escherichia coli: mutants in conserved and non-conserved regions. Biometals 15:121–131

    PubMed  CAS  Google Scholar 

  26. Cobessi D, Celia H, Folschweiller N, Schalk IJ, Abdallah MA, Pattus F (2005a) The crystal structure of the pyoverdine outer membrane receptor FpvA from Pseudomonas aeruginosa at 3.6 angstroms resolution. J Mol Biol 347:121–134

    PubMed  CAS  Google Scholar 

  27. Cobessi D, Celia H, Pattus F (2005b) Crystal structure at high resolution of ferric-pyochelin and its membrane receptor FptA from Pseudomonas aeruginosa. J Mol Biol 352:893–904

    PubMed  CAS  Google Scholar 

  28. Cornelissen CN (2003) Transferrin-iron uptake by Gram-negative bacteria. Front Biosci 8:d836–d847

    PubMed  CAS  Google Scholar 

  29. Crosa JH (1997) Signal transduction and transcriptional and posttranscriptional control of iron-regulated genes in bacteria. Microbiol Mol Biol Rev 61:319–336

    PubMed  CAS  Google Scholar 

  30. Cwerman H, Wandersman C, Biville F (2006) Heme and a five-amino-acid hemophore region form the bipartite stimulus triggering the has signaling cascade. J Bacteriol 188:3357–3364

    PubMed  CAS  Google Scholar 

  31. Dashper SG, Butler CA, Lissel JP, Paolini RA, Hoffmann B, Veith PD, O'Brien-Simpson NM, Snelgrove SL, Tsiros JT, Reynolds EC (2005) A novel Porphyromonas gingivalis FeoB plays a role in manganese accumulation. J Biol Chem 280:28095–28102

    PubMed  CAS  Google Scholar 

  32. de Lorenzo V, Wee S, Herrero M, Neilands JB (1987) Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor. J Bacteriol 169:2624–2630

    PubMed  Google Scholar 

  33. de Lorenzo V, Prez-Martin J, Escolar L, Pesole G, Bertoni G (2004) Mode of binding of the Fur protein to target DNA: negative regulation of iron-controlled gene expression. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington, DC, pp 185–196

    Google Scholar 

  34. Dean CR, Neshat S, Poole K (1996) PfeR, an enterobactin-responsive activator of ferric enterobactin receptor gene expression in Pseudomonas aeruginosa. J Bacteriol 178:5361–5369

    PubMed  CAS  Google Scholar 

  35. Dhungana S, Anderson DS, Mietzner TA, Crumbliss AL (2005) Kinetics of iron release from ferric binding protein (FbpA): mechanistic implications in bacterial periplasm-to-cytosol Fe3+transport. Biochemistry 44:9606–9618

    PubMed  CAS  Google Scholar 

  36. Diaz-Mireles E, Wexler M, Todd JD, Bellini D, Johnston AW, Sawers RG (2005) The manganese-responsive repressor Mur of Rhizobium leguminosarum is a member of the Fur-superfamily that recognizes an unusual operator sequence. Microbiology 151:4071–4078

    PubMed  CAS  Google Scholar 

  37. Endriss F, Braun V (2004) Loop deletions indicate regions important for FhuA transport and receptor functions in Escherichia coli. J Bacteriol 186:4818–4823

    PubMed  CAS  Google Scholar 

  38. Enz S, Brand H, Orellana C, Mahren S, Braun V (2003a) Sites of interaction between the FecA and FecR signal transduction proteins of ferric citrate transport in Escherichia coli K-12. J Bacteriol 185:3745–3752

    PubMed  CAS  Google Scholar 

  39. Enz S, Braun V, Crosa JH (1995) Transcription of the region encoding the ferric dicitrate-transport system in Escherichia coli: similarity between promoters for fecA and for extracytoplasmic function sigma factors. Gene 163:13–18

    PubMed  CAS  Google Scholar 

  40. Enz S, Mahren S, Menzel C, Braun V (2003b) Analysis of the ferric citrate transport gene promoter of Escherichia coli. J Bacteriol 185:2387–2391

    PubMed  CAS  Google Scholar 

  41. Enz S, Mahren S, Stroeher UH, Braun V (2000) Surface signaling in ferric citrate transport gene induction: interaction of the FecA, FecR, and FecI regulatory proteins. J Bacteriol 182:637–646

    PubMed  CAS  Google Scholar 

  42. Faraldo-Gomez JD, Sansom MS (2003) Acquisition of siderophores in Gram-negative bacteria. Nat Rev Mol Cell Biol 4:105–116

    PubMed  CAS  Google Scholar 

  43. Ferguson AD, Chakraborty R, Smith BS, Esser L, van der HD, Deisenhofer J (2002) Structural basis of gating by the outer membrane transporter FecA. Science 295:1715–1719

    PubMed  CAS  Google Scholar 

  44. Ferguson AD, Deisenhofer J (2004) Metal import through microbial membranes. Cell 116:15–24

    PubMed  CAS  Google Scholar 

  45. Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W (1998) Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282:2215–2220

    PubMed  CAS  Google Scholar 

  46. Garcia-Herrero A, Vogel HJ (2005) Nuclear magnetic resonance solution structure of the periplasmic signalling domain of the TonB-dependent outer membrane transporter FecA from Escherichia coli. Mol Microbiol 58:1226–1237

    PubMed  CAS  Google Scholar 

  47. Geissmann TA, Touati D (2004) Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J 23:396–405

    PubMed  CAS  Google Scholar 

  48. Gong S, Bearden SW, Geoffroy VA, Fetherston JD, Perry RD (2001) Characterization of the Yersinia pestis Yfu ABC inorganic iron transport system. Infect Immun 69:2829–2837

    PubMed  CAS  Google Scholar 

  49. Grass G, Franke S, Taudte N, Nies DH, Kucharski LM, Maguire ME, Rensing C (2005) The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J Bacteriol 187:1604–1611

    PubMed  CAS  Google Scholar 

  50. Grass G, Wong MD, Rosen BP, Smith RL, Rensing C (2002) ZupT is a Zn(II) uptake system in Escherichia coli. J Bacteriol 184:864–866

    PubMed  CAS  Google Scholar 

  51. Hantke K (1987a) Ferrous iron transport mutants in Escherichia coli K-12. FEMS Microbiol Lett 44:53–57

    CAS  Google Scholar 

  52. Hantke K (1987b) Selection procedure for deregulated iron transport mutants (fur) in Escherichia coli K-12: fur not only affects iron metabolism. Mol Gen Genet 210:135–139

    PubMed  CAS  Google Scholar 

  53. Hantke K (2001) Iron and metal regulation in bacteria. Curr Opin Microbiol 4:172–177

    PubMed  CAS  Google Scholar 

  54. Heinrichs DE, Poole K (1996) PchR, a regulator of ferripyochelin receptor gene (fptA) expression in Pseudomonas aeruginosa, functions both as an activator and as a repressor. J Bacteriol 178:2586–2592

    PubMed  CAS  Google Scholar 

  55. Hoegy F, Celia H, Mislin GL, Vincent M, Gallay J, Schalk IJ (2005) Binding of iron-free siderophore, a common feature of siderophore outer membrane transporters of Escherichia coli and Pseudomonas aeruginosa. J Biol Chem 280:20222–20230

    PubMed  CAS  Google Scholar 

  56. James HE, Beare PA, Martin LW, Lamont IL (2005) Mutational analysis of a bifunctional ferrisiderophore receptor and signal-transducing protein from Pseudomonas aeruginosa. J Bacteriol 187:4514–4520

    PubMed  CAS  Google Scholar 

  57. Jin B, Newton SM, Shao Y, Jiang X, Charbit A, Klebba PE (2006) Iron acquisition systems for ferric hydroxamates, haemin and haemoglobin in Listeria monocytogenes. Mol Microbiol 59:1185–1198

    PubMed  CAS  Google Scholar 

  58. Kammler M, Schön C, Hantke K (1993) Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol 175:6212–6219

    PubMed  CAS  Google Scholar 

  59. Katoh H, Hagino N, Grossman AR, Ogawa T (2001) Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183:2779–2784

    PubMed  CAS  Google Scholar 

  60. Kehres DG, Janakiraman A, Slauch JM, Maguire ME (2002) SitABCD is the alkaline Mn(2+) transporter of Salmonella enterica serovar Typhimurium. J Bacteriol 184:3159–3166

    PubMed  CAS  Google Scholar 

  61. Kempf B, Gade J, Bremer E (1997) Lipoprotein from the osmoregulated ABC transport system OpuA of Bacillus subtilis: purification of the glycine betaine binding protein and characterization of a functional lipidless mutant. J Bacteriol 179:6213–6220

    PubMed  CAS  Google Scholar 

  62. Kim I, Stiefel A, Plantor S, Angerer A, Braun V (1997) Transcription induction of the ferric citrate transport genes via the N-terminus of the FecA outer membrane protein, the Ton system and the electrochemical potential of the cytoplasmic membrane. Mol Microbiol 23:333–344

    PubMed  CAS  Google Scholar 

  63. Kirby AE, King ND, Connell TD (2004) RhuR, an extracytoplasmic function sigma factor activator, is essential for heme-dependent expression of the outer membrane heme and hemoprotein receptor of Bordetella avium. Infect Immun 72:896–907

    PubMed  CAS  Google Scholar 

  64. Klebba PE (2003) Three paradoxes of ferric enterobactin uptake. Front Biosci 8:s1422–s1436

    PubMed  CAS  Google Scholar 

  65. Ködding J, Killig F, Polzer P, Howard SP, Diedrichs K, Welte W (2005) Crystal structure of a 92-residue C-terminal fragment of TonB from Escherichia coli reveals significant conformational changes compared to structures of smaller TonB fragments. J Biol Chem 280:3022–3028

    PubMed  Google Scholar 

  66. Koster M, van Klompenburg W, Bitter W, Leong J, Weisbeek P (1994) Role for the outer membrane ferric siderophore receptor PupB in signal transduction across the bacterial cell envelope. EMBO J 13:2805–2813

    PubMed  CAS  Google Scholar 

  67. Köster W (2001) ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B12. Res Microbiol 152:291–301

    PubMed  Google Scholar 

  68. Krewulak KD, Shepherd CM, Vogel HJ (2005) Molecular dynamics simulations of the periplasmic ferric-hydroxamate binding protein FhuD. Biometals 18:375–386

    PubMed  CAS  Google Scholar 

  69. Letoffe S, Delepelaire P, Wandersman C (2004) Free and hemophore-bound heme acquisitions through the outer membrane receptor HasR have different requirements for the TonB-ExbB-ExbD complex. J Bacteriol 186:4067–4074

    PubMed  CAS  Google Scholar 

  70. Letoffe S, Wecker K, Delepierre M, Delepelaire P, Wandersman C (2005) Activities of the Serratia marcescens heme receptor HasR and isolated plug and beta-barrel domains: the beta-barrel forms a heme-specific channel. J Bacteriol 187:4637–4645

    PubMed  CAS  Google Scholar 

  71. Leveille S, Caza M, Johnson JR, Clabots C, Sabri M, Dozois CM (2006) Iha from an Escherichia coli urinary tract infection outbreak clonal group A strain is expressed in vivo in the mouse urinary tract and functions as a catecholate siderophore receptor. Infect Immun 74:3427–3436

    PubMed  CAS  Google Scholar 

  72. Liu M, Lei B (2005) Heme transfer from streptococcal cell surface protein Shp to HtsA of transporter HtsABC. Infect Immun 73:5086–5092

    PubMed  CAS  Google Scholar 

  73. Llamas MA, Sparrius M, Kloet R, Jimenez CR, Vandenbroucke-Grauls C, Bitter W (2006) The heterologous siderophores ferrioxamine B and ferrichrome activate signaling pathways in Pseudomonas aeruginosa. J Bacteriol 188:1882–1891

    PubMed  CAS  Google Scholar 

  74. Locher KP, Lee AT, Rees DC (2002) The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296:1091–1098

    PubMed  CAS  Google Scholar 

  75. Locher KP, Rees B, Koebnik R, Mitschler A, Moulinier L, Rosenbusch JP, Moras D (1998) Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95:771–778

    PubMed  CAS  Google Scholar 

  76. Louvel H, Saint GI, Picardeau M (2005) Isolation and characterization of FecA- and FeoB-mediated iron acquisition systems of the spirochete Leptospira biflexa by random insertional mutagenesis. J Bacteriol 187:3249–3254

    PubMed  CAS  Google Scholar 

  77. Lu G, Westbrooks JM, Davidson AL, Chen J (2005) ATP hydrolysis is required to reset the ATP-binding cassette dimer into the resting-state conformation. Proc Natl Acad Sci USA 102:17969–17974

    PubMed  CAS  Google Scholar 

  78. Luck SN, Turner SA, Rajakumar K, Sakellaris H, Adler B (2001) Ferric dicitrate transport system (Fec) of Shigella flexneri2a YSH6000 is encoded on a novel pathogenicity island carrying multiple antibiotic resistance genes. Infect Immun 69:6012–6021

    PubMed  CAS  Google Scholar 

  79. Mahren S, Schnell H, Braun V (2005) Occurrence and regulation of the ferric citrate transport system in Escherichia coli B, Klebsiella pneumoniae, Enterobacter aerogenes, and Photorhabdus luminescens. Arch Microbiol 184:175–186

    PubMed  CAS  Google Scholar 

  80. Marlovits TC, Haase W, Herrmann C, Aller SG, Unger VM (2002) The membrane protein FeoB contains an intramolecular G protein essential for Fe(II) uptake in bacteria. Proc Natl Acad Sci USA 99:16243–16248

    PubMed  CAS  Google Scholar 

  81. Marraffini LA, Dedent AC, Schneewind O (2006) Sortases and the art of anchoring proteins to the envelopes of Gram-positive bacteria. Microbiol Mol Biol Rev 70:192–221

    PubMed  CAS  Google Scholar 

  82. Masse E, Gottesman S (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci USA 99:4620–4625

    PubMed  CAS  Google Scholar 

  83. Merrell DS, Thompson LJ, Kim CC, Mitchell H, Tompkins LS, Lee A, Falkow S (2003) Growth phase-dependent response of Helicobacter pylori to iron starvation. Infect Immun 71:6510–6525

    PubMed  CAS  Google Scholar 

  84. Mey AR, Wyckoff EE, Kanukurthy V, Fisher CR, Payne SM (2005) Iron and fur regulation in Vibrio cholerae and the role of fur in virulence. Infect Immun 73:8167–8178

    PubMed  CAS  Google Scholar 

  85. Mietzner TA, Tencza SB, Adhikari P, Vaughan KG, Nowalk AJ (1998) Fe(III) periplasm-to-cytosol transporters of Gram-negative pathogens. Curr Top Microbiol Immunol 225:113–135

    PubMed  CAS  Google Scholar 

  86. Oakhill JS, Sutton BJ, Gorringe AR, Evans RW (2005) Homology modelling of transferrin-binding protein A from Neisseria meningitidis. Protein Eng Des Sel 18:221–228

    PubMed  CAS  Google Scholar 

  87. Page RDM (2005) Inferring evolutionary relationships. In: Baxevanis AD, Davison DB, Paghe RDM, Petsko GA, Stein LD, Stormo GD (eds) Current protocols in bioinformatics, Chap. 6. Wiley, New York

    Google Scholar 

  88. Patzer SI, Hantke K (2001) Dual repression by Fe(2+)-Fur and Mn(2+)-MntR of the mntH gene, encoding an NRAMP-like Mn(2+) transporter in Escherichia coli. J Bacteriol 183:4806–4813

    PubMed  CAS  Google Scholar 

  89. Pawelek PD, Croteau N, Ng-Thow-Hing C, Khursigara CM, Moiseeva N, Allaire M, Coulton JW (2006) Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science 312:1399–1402

    PubMed  CAS  Google Scholar 

  90. Peacock RS, Weljie AM, Peter Howard S, Price FD, Vogel HJ (2005) The solution structure of the C-terminal domain of TonB and interaction studies with TonB box peptides. J Mol Biol 345:1185–1197

    CAS  Google Scholar 

  91. Pecqueur L, D'Autreaux B, Dupuy J, Nicolet Y, Jacquamet L, Brutscher B, Michaud-Soret I, Bersch B (2006) Structural changes of E. coli Fur during metal dependent dimerization and activation explored by NMR and X-ray crystallography. J Biol Chem 281:21286–21295

    PubMed  CAS  Google Scholar 

  92. Perkins-Balding D, Ratliff-Griffin M, Stojiljkovic I (2004) Iron transport systems in Neisseria meningitidis. Microbiol Mol Biol Rev 68:154–171

    PubMed  CAS  Google Scholar 

  93. Pohl E, Haller JC, Mijovilovich A, Meyer-Klaucke W, Garman E, Vasil ML (2003) Architecture of a protein central to iron homeostasis: crystal structure and spectroscopic analysis of the ferric uptake regulator. Mol Microbiol 47:903–915

    PubMed  CAS  Google Scholar 

  94. Pohl E, Holmes RK, Hol WG (1999) Crystal structure of a cobalt-activated diphtheria toxin repressor-DNA complex reveals a metal-binding SH3-like domain. J Mol Biol 292:653–667

    PubMed  CAS  Google Scholar 

  95. Postle K, Kadner RJ (2003) Touch and go: tying TonB to transport. Mol Microbiol 49:869–882

    PubMed  CAS  Google Scholar 

  96. Prakash S, Cooper G, Singhi S, Saier MH Jr (2003) The ion transporter superfamily. Biochim Biophys Acta 1618:79–92

    PubMed  CAS  Google Scholar 

  97. Pramanik A, Braun V (2006) Albomycin uptake via a ferric hydroxamate transport system of Streptococcus pneumoniae R6. J Bacteriol 188:3878–3886

    PubMed  CAS  Google Scholar 

  98. Qi Z, Hamza I, O'Brian MR (1999) Heme is an effector molecule for iron-dependent degradation of the bacterial iron response regulator (Irr) protein. Proc Natl Acad Sci USA 96:13056–13061

    PubMed  CAS  Google Scholar 

  99. Raphael BH, Joens LA (2003) FeoB is not required for ferrous iron uptake in Campylobacter jejuni. Can J Microbiol 49:727–731

    PubMed  CAS  Google Scholar 

  100. Raymond KN, Dertz EA, Kim SS (2003) Enterobactin: an archetype for microbial iron transport. Proc Natl Acad Sci USA 100:3584–3588

    PubMed  CAS  Google Scholar 

  101. Redly GA, Poole K (2005) FpvIR control of fpvA ferric pyoverdine receptor gene expression in Pseudomonas aeruginosa: demonstration of an interaction between FpvI and FpvR and identification of mutations in each compromising this interaction. J Bacteriol 187:5648–5657

    PubMed  CAS  Google Scholar 

  102. Rodriguez GM, Voskuil MI, Gold B, Schoolnik GK, Smith I (2002) ideR, an essential gene in Mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect Immun 70:3371–3381

    PubMed  CAS  Google Scholar 

  103. Rohde KH, Dyer DW (2003) Mechanisms of iron acquisition by the human pathogens Neisseria meningitidis and Neisseria gonorrhoeae. Front Biosci 8:d1186–d1218

    PubMed  CAS  Google Scholar 

  104. Rohrbach MR, Braun V, Köster W (1995) Ferrichrome transport in Escherichia coli K-12: altered substrate specificity of mutated periplasmic FhuD and interaction of FhuD with the integral membrane protein FhuB. J Bacteriol 177:7186–7193

    PubMed  CAS  Google Scholar 

  105. Rudolph G, Hennecke H, Fischer HM (2006) Beyond the Fur paradigm: iron-controlled gene expression in rhizobia. FEMS Microbiol Rev 30:631–648

    PubMed  CAS  Google Scholar 

  106. Runyen-Janecky LJ, Reeves SA, Gonzales EG, Payne SM (2003) Contribution of the Shigella flexneri Sit, Iuc, and Feo iron acquisition systems to iron acquisition in vitro and in cultured cells. Infect Immun 71:1919–1928

    PubMed  CAS  Google Scholar 

  107. Sabri M, Leveille S, Dozois CM (2006) A SitABCD homologue from an avian pathogenic Escherichia coli strain mediates transport of iron and manganese and resistance to hydrogen peroxide. Microbiology 152:745–758

    PubMed  CAS  Google Scholar 

  108. Saken E, Rakin A, Heesemann J (2000) Molecular characterization of a novel siderophore-independent iron transport system in Yersinia. Int J Med Microbiol 290:51–60

    PubMed  CAS  Google Scholar 

  109. Sauter A, Braun V (2004) Defined inactive FecA derivatives mutated in functional domains of the outer membrane transport and signaling protein of Escherichia coli K-12. J Bacteriol 186:5303–5310

    PubMed  CAS  Google Scholar 

  110. Schalk IJ, Yue WW, Buchanan SK (2004) Recognition of iron-free siderophores by TonB-dependent iron transporters. Mol Microbiol 54:14–22

    PubMed  CAS  Google Scholar 

  111. Schneider R, Hantke K (1993) Iron-hydroxamate uptake systems in Bacillus subtilis: identification of a lipoprotein as a part of a binding protein-dependent transport system. Mol Microbiol 8:111–121

    PubMed  CAS  Google Scholar 

  112. Scott DC, Cao Z, Qi Z, Bauler M, Igo JD, Newton SM, Klebba PE (2001) Exchangeability of N-termini in the ligand-gated porins of Escherichia coli. J Biol Chem 276:13025–13033

    PubMed  CAS  Google Scholar 

  113. Scott DC, Newton SM, Klebba PE (2002) Surface loop motion in FepA. J Bacteriol 184:4906–4911

    PubMed  CAS  Google Scholar 

  114. Sebulsky MT, Speziali CD, Shilton BH, Edgell DR, Heinrichs DE (2004) FhuD1, a ferric hydroxamate-binding lipoprotein in Staphylococcus aureus: a case of gene duplication and lateral transfer. J Biol Chem 279:53152–53159

    PubMed  CAS  Google Scholar 

  115. Shen J, Meldrum A, Poole K (2002) FpvA receptor involvement in pyoverdine biosynthesis in Pseudomonas aeruginosa. J Bacteriol 184:3268–3275

    PubMed  CAS  Google Scholar 

  116. Shouldice SR, Dougan DR, Skene RJ, Tari LW, McRee DE, Yu RH, Schryvers AB (2003) High-resolution structure of an alternate form of the ferric ion-binding protein from Haemophilus influenzae. J Biol Chem 278:11513–11519

    PubMed  CAS  Google Scholar 

  117. Shultis DD, Purdy MD, Banchs CN, Wiener MC (2006) Outer membrane active transport: structure of the BtuB:TonB complex. Science 312:1396–1399

    PubMed  CAS  Google Scholar 

  118. Stiefel A, Mahren S, Ochs M, Schindler PT, Enz S, Braun V (2001) Control of the ferric citrate transport system of Escherichia coli: mutations in region 2.1 of the FecI extracytoplasmic-function sigma factor suppress mutations in the FecR transmembrane regulatory protein. J Bacteriol 183:162–170

    PubMed  CAS  Google Scholar 

  119. Suzuki T, Okamura Y, Calugay RJ, Takeyama H, Matsunaga T (2006) Global gene expression analysis of iron-inducible genes in Magnetospirillum magneticum AMB-1. J Bacteriol 188:2275–2279

    PubMed  CAS  Google Scholar 

  120. Tarr PI, Bilge SS, Vary JC Jr., Jelacic S, Habeeb RL, Ward TR, Baylor MR, Besser TE (2000) Iha: a novel Escherichia coli O157: H7 adherence-conferring molecule encoded on a recently acquired chromosomal island of conserved structure. Infect Immun 68:1400–1407

    PubMed  CAS  Google Scholar 

  121. Todd JD, Wexler M, Sawers G, Yeoman KH, Poole PS, Johnston AW (2002) RirA, an iron-responsive regulator in the symbiotic bacterium Rhizobium leguminosarum. Microbiology 148:4059–4071

    PubMed  CAS  Google Scholar 

  122. Van Gelder P, Dumas F, Bartoldus I, Saint N, Prilipov A, Winterhalter M, Wang Y, Philippsen A, Rosenbusch JP, Schirmer T (2002) Sugar transport through maltoporin of Escherichia coli: role of the greasy slide. J Bacteriol 184:2994–2999

    PubMed  Google Scholar 

  123. Vanderpool CK, Armstrong SK (2004) Integration of environmental signals controls expression of Bordetella heme utilization genes. J Bacteriol 186:938–948

    PubMed  CAS  Google Scholar 

  124. Velayudhan J, Hughes NJ, McColm AA, Bagshaw J, Clayton CL, Andrews SC, Kelly DJ (2000) Iron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporter. Mol Microbiol 37:274–286

    PubMed  CAS  Google Scholar 

  125. Waidner B, Greiner S, Odenbreit S, Kavermann H, Velayudhan J, Stahler F, Guhl J, Bisse E, van Vliet AH, Andrews SC, Kusters JG, Kelly DJ, Haas R, Kist M, Bereswill S (2002) Essential role of ferritin Pfr in Helicobacter pylori iron metabolism and gastric colonization. Infect Immun 70:3923–3929

    PubMed  CAS  Google Scholar 

  126. Wandersman C, Delepelaire P (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647

    PubMed  CAS  Google Scholar 

  127. Watnick PI, Butterton JR, Calderwood SB (1998) The interaction of the Vibrio cholerae transcription factors, Fur and IrgB, with the overlapping promoters of two virulence genes, irgA and irgB. Gene 209:65–70

    PubMed  CAS  Google Scholar 

  128. Wexler M, Todd JD, Kolade O, Bellini D, Hemmings AM, Sawers G, Johnston AW (2003) Fur is not the global regulator of iron uptake genes in Rhizobium leguminosarum. Microbiology 149:1357–1365

    PubMed  CAS  Google Scholar 

  129. Wilson MJ, Lamont IL (2006) Mutational analysis of an extracytoplasmic-function sigma factor to investigate its interactions with RNA polymerase and DNA. J Bacteriol 188:1935–1942

    PubMed  CAS  Google Scholar 

  130. Winkelmann et al. (1991) CRC handbook of microbial iron chelates. CRC Press, Boca Raton, FL

    Google Scholar 

  131. Wyckoff EE, Lopreato GF, Tipton KA, Payne SM (2005) Shigella dysenteriae ShuS promotes utilization of heme as an iron source and protects against heme toxicity. J Bacteriol 187:5658–5664

    PubMed  CAS  Google Scholar 

  132. Wyckoff EE, Schmitt M, Wilks A, Payne SM (2004) HutZ is required for efficient heme utilization in Vibrio cholerae. J Bacteriol 186:4142–4151

    PubMed  CAS  Google Scholar 

  133. Yang J, Sangwan I, Lindemann A, Hauser F, Hennecke H, Fischer HM, O'Brian MR (2006) Bradyrhizobium japonicum senses iron through the status of haem to regulate iron homeostasis and metabolism. Mol Microbiol 60:427–437

    PubMed  Google Scholar 

  134. Yue WW, Grizot S, Buchanan SK (2003) Structural evidence for iron-free citrate and ferric citrate binding to the TonB-dependent outer membrane transporter FecA. J Mol Biol 332:353–368

    PubMed  CAS  Google Scholar 

  135. Zhou D, Hardt WD, Galan JE (1999) Salmonella typhimurium encodes a putative iron transport system within the centisome 63 pathogenicity island. Infect Immun 67:1974–1981

    PubMed  CAS  Google Scholar 

  136. Zimmermann L, Angerer A, Braun V (1989) Mechanistically novel iron(III) transport system in Serratia marcescens. J Bacteriol 171:238–243

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Volkmar Braun .

Editor information

Dietrich H. Nies Simon Silver

Rights and permissions

Reprints and permissions

Copyright information

© 2007 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Braun, V., Hantke, K. (2007). Acquisition of Iron by Bacteria. In: Nies, D.H., Silver, S. (eds) Molecular Microbiology of Heavy Metals. Microbiology Monographs, vol 6. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7171_2006_078

Download citation

Publish with us

Policies and ethics