, 20:303

Bordetella iron transport and virulence

  • Timothy J. Brickman
  • Mark T. Anderson
  • Sandra K. Armstrong


Bordetella pertussis, Bordetella parapertussis, and Bordetella bronchiseptica are pathogens with a complex iron starvation stress response important for adaptation to nutrient limitation and flux in the mammalian host environment. The iron starvation stress response is globally regulated by the Fur repressor using ferrous iron as the co-repressor. Expression of iron transport system genes of Bordetella is coordinated by priority regulation mechanisms that involve iron source sensing. Iron source sensing is mediated by distinct transcriptional activators that are responsive to the cognate iron source acting as the inducer.


Bordetella Iron Heme Siderophore 


  1. Agiato LA, Dyer DW (1992) Siderophore production and membrane alterations by Bordetella pertussis in response to iron starvation. Infect Immun 60:117–123PubMedGoogle Scholar
  2. Anderson MT, Armstrong SK (2004) The BfeR regulator mediates enterobactin-inducible expression of Bordetella enterobactin utilization genes. J Bacteriol 186:7302–7311CrossRefPubMedGoogle Scholar
  3. Anderson MT, Armstrong SK (2006) The Bordetella Bfe system: growth and transcriptional response to siderophores, catechols, and neuroendocrine catecholamines. J Bacteriol 188:5731–5740Google Scholar
  4. Anderton TL, Maskell DJ, Preston A (2004) Ciliostasis is a key early event during colonization of canine tracheal tissue by Bordetella bronchiseptica. Microbiology 150:2843–2855CrossRefPubMedGoogle Scholar
  5. Antoine R, Alonso S, Raze D et al (2000) New virulence-activated and virulence-repressed genes identified by systematic gene inactivation and generation of transcriptional fusions in Bordetella pertussis. J Bacteriol 182:5902–5905CrossRefPubMedGoogle Scholar
  6. Armstrong SK, Clements MO (1993) Isolation and characterization of Bordetella bronchiseptica mutants deficient in siderophore activity. J Bacteriol 175:1144–1152PubMedGoogle Scholar
  7. Beall B (1998) Two iron-regulated putative ferric siderophore receptor genes in Bordetella bronchiseptica and Bordetella pertussis. Res Microbiol 149:189–201CrossRefPubMedGoogle Scholar
  8. Beall B, Hoenes T (1997) An iron-regulated outer-membrane protein specific to Bordetella bronchiseptica and homologous to ferric siderophore receptors. Microbiology 143(Pt 1):135–145CrossRefPubMedGoogle Scholar
  9. Beall B, Sanden GN (1995a) A Bordetella pertussis fepA homologue required for utilization of exogenous ferric enterobactin. Microbiology 141:3193–3205CrossRefGoogle Scholar
  10. Beall BW, Sanden GN (1995b) Cloning and initial characterization of the Bordetella pertussis fur gene. Curr Microbiol 30:223–226CrossRefGoogle Scholar
  11. 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 180:862–870PubMedGoogle Scholar
  12. Bergeron RJ, McManis JS, Perumal PT, Algee SE (1991). The total synthesis of alcaligin. J Org Chem 56:5560–5563CrossRefGoogle Scholar
  13. Bister B, Bischoff D, Nicholson GJ et al (2004) The structure of salmochelins: C-glucosylated enterobactins of Salmonella enterica. Biometals 17:471–481CrossRefPubMedGoogle Scholar
  14. Bordet J, Gengou O (1906) Le microbe de la coqueluche. Ann Inst Pasteur (Paris) 20:731–741Google Scholar
  15. Boukhalfa H, Brickman TJ, Armstrong SK, Crumbliss AL (2000) Kinetics and mechanism of iron(III) dissociation from the dihydroxamate siderophores alcaligin and rhodotorulic acid. Inorg Chem 39:5591–5602CrossRefPubMedGoogle Scholar
  16. Boukhalfa H, Crumbliss AL (2000) Multiple-path dissociation mechanism for mono- and dinuclear tris(hydroxamato)iron(III) complexes with dihydroxamic acid ligands in aqueous solution. Inorg Chem 39:4318–4331CrossRefPubMedGoogle Scholar
  17. Braun V, Mahren S (2005). Transmembrane transcriptional control (surface signalling) of the Escherichia coli Fec type. FEMS Microbiol Rev 29:673–684CrossRefPubMedGoogle Scholar
  18. Brickman TJ, Armstrong SK (1995) Bordetella pertussis fur gene restores iron repressibility of siderophore and protein expression to deregulated Bordetella bronchiseptica mutants. J Bacteriol 177:268–270PubMedGoogle Scholar
  19. Brickman TJ, Armstrong SK (1996). The ornithine decarboxylase gene odc is required for alcaligin siderophore biosynthesis in Bordetella spp.: putrescine is a precursor of alcaligin. J Bacteriol 178:54–60PubMedGoogle Scholar
  20. Brickman TJ, Armstrong SK (1999) Essential role of the iron-regulated outer membrane receptor FauA in alcaligin siderophore-mediated iron uptake in Bordetella species. J Bacteriol 181:5958–5966PubMedGoogle Scholar
  21. Brickman TJ, Armstrong SK (2002). Bordetella interspecies allelic variation in AlcR inducer requirements: identification of a critical determinant of AlcR inducer responsiveness and construction of an alcR(Con) mutant allele. J Bacteriol 184:1530–1539CrossRefPubMedGoogle Scholar
  22. Brickman TJ, Armstrong SK (2005). Bordetella AlcS transporter functions in alcaligin siderophore export and is central to inducer sensing in positive regulation of alcaligin system gene expression. J Bacteriol 187:3650–3661CrossRefPubMedGoogle Scholar
  23. Brickman TJ, Hansel JG, Miller MJ, Armstrong SK (1996) Purification, spectroscopic analysis and biological activity of the macrocyclic dihydroxamate siderophore alcaligin produced by Bordetella pertussis and Bordetella bronchiseptica. Biometals 9:191–203CrossRefPubMedGoogle Scholar
  24. Brickman TJ, Kang HY, Armstrong SK (2001) Transcriptional activation of Bordetella alcaligin siderophore genes requires the AlcR regulator with alcaligin as inducer. J Bacteriol 183:483–489CrossRefPubMedGoogle Scholar
  25. Brickman TJ, McIntosh MA (1992) Overexpression and purification of ferric enterobactin esterase from Escherichia coli. Demonstration of enzymatic hydrolysis of enterobactin and its iron complex. J Biol Chem 267:12350–12355PubMedGoogle Scholar
  26. Brickman TJ, Vanderpool CK, Armstrong SK (2006) Heme transport contributes to in␣vivo fitness of Bordetella pertussis during primary infection in mice. Infect Immun 74:1741–1744CrossRefPubMedGoogle Scholar
  27. Bruss JB, Siber GR (1999) Protective effects of pertussis immunoglobulin (P-IGIV) in the aerosol challenge model. Clin Diagn Lab Immunol 6:464–470PubMedGoogle Scholar
  28. Budzikiewicz H, Bössenkamp A, Taraz K, Pandey A, Meyer JM (1997) Corynebactin, a cyclic catecholate siderophore from Corynebacterium glutamicum ATCC 14067 (Brevibacterium sp. DSM 20411). Z Naturforsch 52:551–554Google Scholar
  29. Burton CL, Chhabra SR, Swift S et al (2002). The growth response of Escherichia coli to neurotransmitters and related catecholamine drugs requires a functional enterobactin biosynthesis and uptake system. Infect Immun 70:5913–5923CrossRefPubMedGoogle Scholar
  30. Carson SDB, Klebba PE, Newton SM, Sparling PF (1999) Ferric enterobactin binding and utilization by Neisseria gonorrhoeae. J Bacteriol 181:2895–2901PubMedGoogle Scholar
  31. Centers, for, Disease, Control, and, Prevention (2002) Pertussis - United States, 1997–2000. MMWR Morb Mortal Wkly Rep 51:73–76Google Scholar
  32. Centers, for, Disease, Control, and, Prevention (2006) Preventing tetanus, diphtheria, and pertussis among adolescents: use of tetanus toxoid, reduced diphtheria toxoid and acellular pertussis vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 55:1–46Google Scholar
  33. Challis GL (2005) A widely distributed bacterial pathway for siderophore biosynthesis independent of nonribosomal peptide synthetases. Chembiochem: Eur J Chem Biol 6:601–611CrossRefGoogle Scholar
  34. Cherry JD, Heininger U (2004) Pertussis and other Bordetella infections. In: Feigin RD, Cherry JD, Demmler GJ, Kaplan S (eds) Textbook of pediatric infectious diseases, 5th edn. The W. B. Saunders Co, Philadelphia, pp 1588–1608Google Scholar
  35. de Lorenzo V, Bindereif A, Paw BH, Neilands JB (1986) Aerobactin biosynthesis and transport genes of plasmid ColV-K30 in Escherichia coli K-12. J Bacteriol 165:570–578PubMedGoogle Scholar
  36. de Lorenzo V, Neilands JB (1986) Characterization of iucA and iucC genes of the aerobactin system of plasmid ColV-K30 in Escherichia coli. J Bacteriol 167:350–355PubMedGoogle Scholar
  37. 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 182:637–646CrossRefPubMedGoogle Scholar
  38. Fetherston JD, Bearden SW, Perry RD (1996) YbtA, an AraC-type regulator of the Yersinia pestis pesticin/yersiniabactin receptor. Mol Microbiol 22:315–325CrossRefPubMedGoogle Scholar
  39. Fiedler HP, Krastel P, Muller J, Gebhardt K, Zeeck A (2001) Enterobactin: the characteristic catecholate siderophore of Enterobacteriaceae is produced by Streptomyces species. FEMS Microbiol Lett 196:147–151PubMedGoogle Scholar
  40. Flak TA, Goldman WE (1999) Signalling and cellular specificity of airway nitric oxide production in pertussis. Cell Microbiol 1:51–60CrossRefPubMedGoogle Scholar
  41. Freestone PP, Lyte M, Neal CP, Maggs AF, Haigh RD, Williams PH (2000) The mammalian neuroendocrine hormone norepinephrine supplies iron for bacterial growth in the presence of transferrin or lactoferrin. J␣Bacteriol 182:6091–6098CrossRefPubMedGoogle Scholar
  42. Gallegos MT, Schleif R, Bairoch A, Hofmann K, Ramos JL (1997) Arac/XylS family of transcriptional regulators. Microbiol Mol Biol Rev 61:393–410PubMedGoogle Scholar
  43. Giardina PC, Foster L-A, Toth SI, Roe BA, Dyer DW (1995) Identification of alcA, a Bordetella bronchiseptica gene necessary for alcaligin production. Gene 167:133–136CrossRefPubMedGoogle Scholar
  44. Giardina PC, Foster LA, Toth SI, Roe BA, Dyer DW (1997) Analysis of the alcABC operon encoding alcaligin biosynthesis enzymes in Bordetella bronchiseptica. Gene 194:19–24CrossRefPubMedGoogle Scholar
  45. Granstrom M, Olinder-Nielsen AM, Holmblad P, Mark A, Hanngren K (1991) Specific immunoglobulin for treatment of whooping cough. Lancet 338:1230–1233CrossRefPubMedGoogle Scholar
  46. Harle C, Kim I, Angerer A, Braun V (1995) Signal transfer through three compartments: transcription initiation of the Escherichia coli ferric citrate transport system from the cell surface. EMBO J 14:1430–1438PubMedGoogle Scholar
  47. Heinrichs DE, Poole K (1993) Cloning and sequence analysis of a gene (pchR) encoding an AraC family activator of pyochelin and ferripyochelin receptor synthesis in Pseudomonas aeruginosa. J Bacteriol 175:5882–5889PubMedGoogle Scholar
  48. 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 178:2586–2592PubMedGoogle Scholar
  49. Hewlett EL, Donato GM, Gray MC (2006) Macrophage cytotoxicity produced by adenylate cyclase toxin from Bordetella pertussis: more than just making cyclic AMP! Mol Microbiol 59:447–459CrossRefPubMedGoogle Scholar
  50. Hou Z, Raymond KN, O’Sullivan B, Esker TW, Nishio T (1998) A preorganized siderophore: thermodynamic and structural characterization of alcaligin and bisucaberin, microbial macrocyclic dihydroxamate chelating agents (1). Inorg Chem 37:6630–6637CrossRefPubMedGoogle Scholar
  51. Hou Z, Sunderland CJ, Nishio T, Raymond KN (1996) Preorganization of ferric alcaligin, Fe2L3. the first structure of a ferric dihydroxamate siderophore. J␣Amer Chem Soc 118:5148–5149CrossRefGoogle Scholar
  52. Kameyama T, Takahashi A, Kurasawa S et al (1987) Bisucaberin, a new siderophore, sensitizing tumor cells to macrophage-mediated cytolysis. I. Taxonomy of the producing organism, isolation and biological properties. J Antibiot 40:1664–1670PubMedGoogle Scholar
  53. Kang HY, Armstrong SK (1998) Transcriptional analysis of the Bordetella alcaligin siderophore biosynthesis operon. J Bacteriol 180:855–861PubMedGoogle Scholar
  54. Kang HY, Brickman TJ, Beaumont FC, Armstrong SK (1996) Identification and characterization of iron-regulated Bordetella pertussis alcaligin siderophore biosynthesis genes. J Bacteriol 178:4877–4884PubMedGoogle Scholar
  55. 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 23:333–344CrossRefPubMedGoogle Scholar
  56. Kirby AE, Metzger DJ, Murphy ER, Connell TD (2001) Heme utilization in Bordetella avium is regulated by RhuI, a heme-responsive extracytoplasmic function sigma factor. Infect Immun 69:6951–6961CrossRefPubMedGoogle Scholar
  57. Lagergren J (1963) The white blood cell count and the erythrocyte sedimentation rate in pertussis. Acta Paediatr 52:405–409CrossRefPubMedGoogle Scholar
  58. Langman L, Young IG, Frost GE, Rosenberg H, Gibson F (1972). Enterochelin system of iron transport in Escherichia coli: mutations affecting ferric-enterochelin esterase. J Bacteriol 112:1142–1149PubMedGoogle Scholar
  59. Ledyard KM, Butler A (1997). Structure of putrebactin, a new dihydroxamate siderophore produced by Shewanella putrefaciens. J Biol Inorg Chem 2:93–97CrossRefGoogle Scholar
  60. Loomis LD, Raymond KN (1991) Solution equilibria of enterobactin and metal-enterobactin complexes. Inorg Chem 30:906–911CrossRefGoogle Scholar
  61. Lynch D, O’Brien J, Welch T et al (2001) Genetic organization of the region encoding regulation, biosynthesis, and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti. J␣Bacteriol 183:2576–2585CrossRefPubMedGoogle Scholar
  62. Mattoo S, Cherry JD (2005) Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin Microbiol Rev 18:326–382CrossRefPubMedGoogle Scholar
  63. Menozzi FD, Gantiez C, Locht C (1991) Identification and purification of transferrin- and lactoferrin-binding proteins of Bordetella pertussis and Bordetella bronchiseptica. Infect Immun 59:3982–3988PubMedGoogle Scholar
  64. Mills KH, Barnard A, Watkins J, Redhead K (1993) Cell-mediated immunity to Bordetella pertussis: role of Th1 cells in bacterial clearance in a murine respiratory infection model. Infect Immun 61:399–410PubMedGoogle Scholar
  65. Moore CH, Foster LA, Gerbig DG Jr., Dyer DW, Gibson BW (1995) Identification of alcaligin as the siderophore produced by Bordetella pertussis and B. bronchiseptica. J Bacteriol 177:1116–1118PubMedGoogle Scholar
  66. Munoz JJ, Arai H, Bergman RK, Sadowski PL (1981) Biological activities of crystalline pertussigen from Bordetella pertussis. Infect Immun 33:820–826PubMedGoogle Scholar
  67. Murphy ER, Sacco RE, Dickenson A et al (2002) BhuR, a virulence-associated outer membrane protein of Bordetella avium, is required for the acquisition of iron from heme and hemoproteins. Infect Immun 70:5390–5403CrossRefPubMedGoogle Scholar
  68. Nicholson ML, Beall B (1999) Disruption of tonB in Bordetella bronchiseptica and Bordetella pertussis prevents utilization of ferric siderophores, hemin and hemoglobin as iron sources. Microbiology (Reading, United Kingdom) 145:2453–2461Google Scholar
  69. Nishio T, Ishida Y (1990) Production of dihydroxamate siderophore alcaligin by Alcaligenes xylosoxidans subsp. xylosoxidans. Agr Biol Chem 54:1837–1839Google Scholar
  70. Nishio T, Tanaka N, Hiratake J, Katsube Y, Ishida Y, Oda J (1988) Isolation and structure of the novel dihydroxamate siderophore alcaligin. J Amer Chem Soc 110:8733–8734CrossRefGoogle Scholar
  71. O’Brien IG, Gibson F (1970) The structure of enterochelin and related 2,3-dihydroxy-N-benzoylserine conjugates from Escherichia coli. Biochim Biophys Acta 215:393–402PubMedGoogle Scholar
  72. Palenik B, Brahamsha B, Larimer FW et al (2003) The genome of a motile marine Synechococcus. Nature 424:1037–1042CrossRefPubMedGoogle Scholar
  73. Parkhill J, Sebaihia M, Preston A et al (2003) Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35:32–40CrossRefPubMedGoogle Scholar
  74. Passerini de Rossi BN, Friedman LE, Belzoni CB et al (2003) Vir90, a virulence-activated gene coding for a Bordetella pertussis iron-regulated outer membrane protein. Res Microbiol 154:443–450CrossRefPubMedGoogle Scholar
  75. Passerini de Rossi BN, Friedman LE, Gonzalez Flecha FL, Castello PR, Franco MA, Rossi JP (1999) Identification of Bordetella pertussis virulence-associated outer membrane proteins. FEMS Microbiol Lett 172:9–13CrossRefPubMedGoogle Scholar
  76. Pradel E, Guiso N, Locht C (1998) Identification of AlcR, an AraC-type regulator of alcaligin siderophore synthesis in Bordetella bronchiseptica and Bordetella pertussis. J Bacteriol 180:871–880PubMedGoogle Scholar
  77. Pradel E, Guiso N, Menozzi FD, Locht C (2000) Bordetella pertussis TonB, a Bvg-independent virulence determinant. Infect Immun 68:1919–1927CrossRefPubMedGoogle Scholar
  78. Pradel E, Locht C (2001) Expression of the putative siderophore receptor gene bfrZ is controlled by the extracytoplasmic-function sigma factor BupI in Bordetella bronchiseptica. J Bacteriol 183:2910–2917CrossRefPubMedGoogle Scholar
  79. Rabsch W, Voigt W, Reissbrodt R, Tsolis RM, Baumler AJ (1999) Salmonella typhimurium IroN and FepA proteins mediate uptake of enterobactin but differ in their specificity for other siderophores. J Bacteriol 181:3610–3612PubMedGoogle Scholar
  80. Redhead K, Hill T, Chart H (1987) Interaction of lactoferrin and transferrins with the outer membrane of Bordetella pertussis. J Gen Microbiol 133:891–898PubMedGoogle Scholar
  81. Regan JC, Tolstoouhov A (1936) Relations of acid base equilibrium to the pathogenesis and treatment of whooping cough. N Y State J Med 36:1075–1087Google Scholar
  82. Register KB, Ducey TF, Brockmeier SL, Dyer DW (2001) Reduced virulence of a Bordetella bronchiseptica siderophore mutant in neonatal swine. Infect Immun 69:2137–2143CrossRefPubMedGoogle Scholar
  83. Rodgers SJ, Lee C, Ng CY, Raymond KN (1987) Ferric ion sequestering agents. 15. Synthesis, solution chemistry, and electrochemistry of a new cationic analogue of enterobactin. Inorg Chem 26:1622–1625CrossRefGoogle Scholar
  84. Rutz JM, Abdullah T, Singh SP, Kalve VI, Klebba PE (1991) Evolution of the ferric enterobactin receptor in gram-negative bacteria. J Bacteriol 173:5964–5974PubMedGoogle Scholar
  85. Spasojevic I, Armstrong SK, Brickman TJ, Crumbliss AL (1999) Electrochemical behavior of the Fe(III) complexes of the cyclic hydroxamate siderophores alcaligin and desferrioxamine E. Inorg Chem 38:449–454CrossRefPubMedGoogle Scholar
  86. Sperandio V, Torres AG, Jarvis B, Nataro JP, Kaper JB (2003) Bacteria-host communication: the language of hormones. Proc Natl Acad Sci USA 100:8951–8956CrossRefPubMedGoogle Scholar
  87. Stainer DW, Scholte MJ (1970) A simple chemically defined medium for the production of phase I Bordetella pertussis. J Gen Microbiol 63:211–220PubMedGoogle Scholar
  88. Stojiljkovic I, Baumler AJ, Hantke K (1994) Fur regulon in gram-negative bacteria. Identification and characterization of new iron-regulated Escherichia coli genes by a Fur titration assay. J Mol Biol 236:531–545CrossRefPubMedGoogle Scholar
  89. Takahashi A, Nakamura H, Kameyama T et al (1987) Bisucaberin, a new siderophore, sensitizing tumor cells to macrophage-mediated cytolysis. II. Physico-chemical properties and structure determination. J␣Antibiot 40:1671–1676PubMedGoogle Scholar
  90. Uhl MA, Miller JF (1994). Autophosphorylation and phosphotransfer in the Bordetella pertussis BvgAS signal transduction cascade. Proc Natl Acad Sci USA 91:1163–1167CrossRefPubMedGoogle Scholar
  91. Vanderpool CK, Armstrong SK (2001) The Bordetella bhu locus is required for heme iron utilization. J Bacteriol 183:4278–4287CrossRefPubMedGoogle Scholar
  92. Vanderpool CK, Armstrong SK (2003) Heme-responsive transcriptional activation of Bordetella bhu genes. J␣Bacteriol 185:909–917CrossRefPubMedGoogle Scholar
  93. Vanderpool CK, Armstrong SK (2004) Integration of environmental signals controls expression of Bordetella heme utilization genes. J Bacteriol 186:938–948CrossRefPubMedGoogle Scholar
  94. Venuti MC, Rastetter WH, Neilands JB (1979) 1,3,5-Tris(N, N′ N′-2,3-dihydroxybenzoyl)aminomethylbenzene, a synthetic iron chelator related to enterobactin. J Med Chem 22:123–124CrossRefPubMedGoogle Scholar
  95. Ward JI, Cherry JD, Chang SJ et al (2005) Efficacy of an acellular pertussis vaccine among adolescents and adults. N Engl J Med 353:1555–1563CrossRefPubMedGoogle Scholar
  96. Weiss AA, Hewlett EL, Myers GA, Falkow S (1983) Tn5-induced mutations affecting virulence factors of Bordetella pertussis. Infect Immun 42:33–41PubMedGoogle Scholar
  97. Weitl FL, Raymond KN (1979) Ferric ion sequestering agents. 1. Hexadentate O-bonding N,N′N″-tris(2,3-dihydroxybenzoyl) derivatives of 1,5,9-triazacyclotridecane and 1,3,5-triaminomethylbenzene. J Amer Chem Soc 101:2728–2731CrossRefGoogle Scholar
  98. Williams P, Morton DJ, Towner KJ, Stevenson P, Griffiths E (1990) Utilization of enterobactin and other exogenous iron sources by Haemophilus influenzae, H. parainfluenzae and H. paraphrophilus. J Gen Microbiol 136:2343–2350PubMedGoogle Scholar
  99. 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 187:5658–5664CrossRefPubMedGoogle Scholar
  100. Zhu M, Valdebenito M, Winkelmann G, Hantke K (2005) Functions of the siderophore esterases IroD and IroE in iron-salmochelin utilization. Microbiology 151:2363–2372CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • Timothy J. Brickman
    • 1
  • Mark T. Anderson
    • 1
  • Sandra K. Armstrong
    • 1
  1. 1.Department of MicrobiologyUniversity of Minnesota Medical SchoolMinneapolisUSA

Personalised recommendations