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Iron acquisition in Vibrio cholerae

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Abstract

Vibrio cholerae, the causative agent of cholera, has an absolute requirement for iron and must obtain this element in the human host as well as in its varied environmental niches. It has multiple systems for iron acquisition, including the TonB-dependent transport of heme, the endogenous siderophore vibriobactin and several siderophores that are produced by other microorganisms. There is also a Feo system for the transport of ferrous iron and an ABC transporter, Fbp, which transports ferric iron. There appears to be at least one additional high affinity iron transport system that has not yet been identified. In iron replete conditions, iron acquisition genes are repressed by Fur. Fur also represses the synthesis of a small, regulatory RNA, RyhB, which negatively regulates genes for iron-containing proteins involved in the tricarboxylic acid cycle and respiration as well as genes for motility and chemotaxis. The redundancy in iron transport systems has made it more difficult to determine the role of individual systems in vivo and in vitro, but it may reflect the overall importance of iron in the growth and survival of V. cholerae.

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References

  • Andrus CR, Walter M, Crosa JH, Payne S (1983) Synthesis of siderophores by pathogenic Vibrio species. Curr Microbiol 9:209–214

    Article  Google Scholar 

  • Bagg A, Neilands JB (1987) Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry 26:5471–5477

    Article  PubMed  CAS  Google Scholar 

  • Beucher M, Sparling PF (1995) Cloning, sequencing, and characterization of the gene encoding FrpB, a major iron-regulated, outer membrane protein of Neisseria gonorrhoeae. J Bacteriol 177:2041–2049

    PubMed  CAS  Google Scholar 

  • Butterton JR, Stoebner JA, Payne SM, Calderwood SB (1992) Cloning, sequencing, and transcriptional regulation of viuA, the gene encoding the ferric vibriobactin receptor of Vibrio cholerae. J Bacteriol 174:3729–3738

    PubMed  CAS  Google Scholar 

  • Butterton JR, Calderwood SB (1994) Identification, cloning, and sequencing of a gene required for ferric vibriobactin utilization by Vibrio cholerae. J Bacteriol 176:5631–5638

    PubMed  CAS  Google Scholar 

  • Butterton JR, Choi MH, Watnick PI, Carroll PA, Calderwood SB (2000) Vibrio cholerae VibF is required for vibriobactin synthesis and is a member of the family of nonribosomal peptide synthetases. J Bacteriol 182:1731–1738

    Article  PubMed  CAS  Google Scholar 

  • Carson SDB, Klebba PE, Newton SMC, Sparling PF (1999) Ferric enterobactin binding and utilization by Neisseria gonorrhoeae. J Bacteriol 181:2895–2901

    PubMed  CAS  Google Scholar 

  • Cartrön ML, Maddocks S, Gillingham P, Craven CJ, Andrews SC (2006) Feo—transport of ferrous iron into bacteria. BioMetals 19:143–157

    Article  PubMed  CAS  Google Scholar 

  • Crosa JH, Walsh CT (2002) Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev 66:223–249

    Article  PubMed  CAS  Google Scholar 

  • Davis BM, Quinones M, Pratt J, Ding Y, Waldor MK (2005) Characterization of the small untranslated RNA RyhB and its regulon in Vibrio cholerae. J Bacteriol 187:4005–4014

    Article  PubMed  CAS  Google Scholar 

  • Di Lorenzo M, Stork M, Alice AR, López CS, Crosa JH (2004) Vibrio. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington DC, pp. 241–255

    Google Scholar 

  • Faruque SM, Albert MJ, Mekalanos JJ (1998) Epidemiology, genetics and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev 62:1301–1314

    PubMed  CAS  Google Scholar 

  • Ghigo J-M, Letoffe S, Wandersman C (1997) A new type of hemophore-dependent heme acquisition system of Serratia marcescens reconstituted in Escherichia coli. J Bacteriol 179:3572–3579

    PubMed  CAS  Google Scholar 

  • Goldberg MB, Boyko SA, Calderwood SB (1990a) Transcriptional regulation by iron of a Vibrio cholerae virulence gene and homology of the gene to the Escherichia coli fur system. J Bacteriol 172:6863–6870

    CAS  Google Scholar 

  • Goldberg MB, DiRita VJ, Calderwood SB (1990b) Identification of an iron-regulated virulence determinant in Vibrio cholerae, using TnphoA mutagenesis. Infect Immun 58:55–60

    CAS  Google Scholar 

  • Goldberg MB, Boyko SA, Calderwood SB (1991) Positive transcriptional regulation of an iron-regulated virulence gene in Vibrio cholerae. Proc Natl Acad Sci USA 88:1125–1129

    Article  PubMed  CAS  Google Scholar 

  • Goldberg MB, Boyko SA, Buttertion JR et al (1992) Characterization of a Vibrio cholerae virulence factor homologous to the family of TonB-dependent proteins. Mol Microbiol 6:2407–2418

    Article  PubMed  CAS  Google Scholar 

  • Grass G, Franke S, Taudte N et al (2005) The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J Bacteriol 187:1604–1611

    Article  PubMed  CAS  Google Scholar 

  • Griffiths GL, Sigel SP, Payne SM, Neilands JB (1984) Vibriobactin, a siderophore from Vibrio cholerae. J Biol Chem 259:383–385

    PubMed  CAS  Google Scholar 

  • Große C, Scherer J, Koch D et al (2006) A new ferrous iron-uptake transporter, EfeU (YcdN), from Escherichia coli. Mol Microbiol 62:120–131

    Article  PubMed  CAS  Google Scholar 

  • Hantke K (1987) Ferrous iron transport mutant in Escherichia coli K12. FEMS Microbiol Lett 44:53–57

    Article  CAS  Google Scholar 

  • Hantke K (1997) Ferrous iron uptake by a magnesium transport system is toxic for Escherichia coli and Salmonella typhimurium. J Bacteriol 179:6201–6204

    PubMed  CAS  Google Scholar 

  • Hantke K (2004) Ferrous iron transport. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. American Society for Microbiology, Washington DC, pp. 178–184

    Google Scholar 

  • Heidelberg JF, Eisen JA, Nelson WC et al (2000) DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406:477–483

    Article  PubMed  CAS  Google Scholar 

  • Henderson DP (1993) Heme iron utilization in Vibrio cholerae: genetics and role in virulence. Ph.D. dissertation. The University of Texas, Austin TX

  • Henderson DP, Payne SM (1993) Cloning and characterization of the Vibrio cholerae genes encoding the utilization of iron from haemin and haemoglobin. Mol Microbiol 7:461–469

    Article  PubMed  CAS  Google Scholar 

  • Henderson DP, Payne SM (1994a) Vibrio cholerae iron transport systems: role of heme and siderophore iron transport in virulence and identification of a gene associated with multiple iron transport systems. Infect Immun 62:5120–5125

    CAS  Google Scholar 

  • Henderson DP, Payne SM (1994b) Characterization of the Vibrio cholerae outer membrane heme transport protein HutA: sequence of the gene, regulation of expression, and homology to the family of TonB-dependent proteins. J Bacteriol 176:3269–3277

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kaper JB, Morris JG, Levine MM (1995) Cholera. Clin Microbiol Rev 8:48–86

    PubMed  CAS  Google Scholar 

  • Keating TA, Marshall CG, Walsh CT (2000) Reconstitution and characterization of the Vibrio cholerae vibriobactin synthetase from VibB, VibE, VibF, and VibH. Biochemistry 39:15522–15530

    Article  PubMed  CAS  Google Scholar 

  • Kehres DG, Janakiraman A, Slauch JM, Maguire ME (2002) SitABCD is the alkaline Mn2+ transporter of Salmonella enterica serovar Typhimurium. J Bacteriol 184:3159–3166

    Article  PubMed  CAS  Google Scholar 

  • Kirby SD, Lainson FA, Donachie W et al (1998) The Pasteurella haemolytica 35 kDa iron-regulated protein is an FbpA homologue. Microbiology 144:3425–3436

    Article  PubMed  CAS  Google Scholar 

  • Litwin CM, Boyko SA, Calderwood SB (1992) Cloning, sequencing, and transcriptional regulation of the Vibrio cholerae fur gene. J Bacteriol 174:1897–1903

    PubMed  CAS  Google Scholar 

  • Litwin CM, Calderwood SB (1994) Analysis of the complexity of gene regulation by Fur in Vibrio cholerae. J Bacteriol 176:240–248

    PubMed  CAS  Google Scholar 

  • Makui H, Roig E, Cole ST et al (2000) Identification of the Escherichia coli K-12 Nramp orthologue (mntH) as a selective divalent metal ion transporter. Mol Microbiol 35:1065–1078

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 26:4620–4625

    Article  CAS  Google Scholar 

  • McHugh JP, Rodriguez-Quinones F, Abdul-Tehrani H et al (2003) Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. J Biol Chem 278:29478–29486

    CAS  Google Scholar 

  • Mey AR, Payne SM (2001) Haem utilization in Vibrio cholerae involves multiple TonB-dependent haem receptors. Mol Microbiol 42:835–849

    Article  PubMed  CAS  Google Scholar 

  • Mey AR, Wyckoff EE, Oglesby A et al (2002) Identification of the Vibrio cholerae enterobactin receptors VctA and IrgA: IrgA is not required for virulence. Infect Immun 70:3419–3426

    Article  PubMed  CAS  Google Scholar 

  • Mey AR, Payne SM (2003) Analysis of residues determining specificity of Vibrio cholerae TonB1 for its receptors. J Bacteriol 185:1195–1207

    Article  PubMed  CAS  Google Scholar 

  • Mey AR, Craig SA, Payne SM (2005a) Characterization of Vibrio cholerae RyhB: the RyhB regulon and role of ryhB in biofilm formation. Infect Immun 73:5706–5719

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Occhino DA, Wyckoff EE, Henderson DP, Wrona TJ, Payne SM (1998) Vibrio cholerae iron transport: haem transport genes are linked to one of two sets of tonB, exbB, exbD genes. Mol Microbiol 29:1493–1507

    Article  PubMed  CAS  Google Scholar 

  • Ochsner UA, Johnson Z, Vasil ML (2000) Genetics and regulation of two distinct haem-uptake systems, phu and has, in Pseudomonas aeruginosa. Microbiology 146:185–198

    PubMed  CAS  Google Scholar 

  • Ong SA, Peterson T, Neilands JB (1979) Agrobactin, a siderophore from Agrobacterium tumefaciens. J Biol Chem 254:1860–1865

    PubMed  CAS  Google Scholar 

  • Reen FJ, Almagro-Moreno S, Ussery D, Boyd EF (2006) The genomic code: inferring Vibrionaceae niche specialization. Nat Rev Microbiol 4:697–704

    Article  PubMed  CAS  Google Scholar 

  • Reidl J, Klose KE (2002) Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiol Rev 26:125–139

    Article  PubMed  CAS  Google Scholar 

  • Rogers MB, Sexton JA, DeCastro GJ, Calderwood SB (2000) Identification of an operon required for ferrichrome iron utilization in Vibrio cholerae. J Bacteriol 182:2350–2353

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sack DA, Sack RB, Chaignat CL (2006) Getting serious about cholera. N Engl J Med 355:649–651

    Article  PubMed  CAS  Google Scholar 

  • Schoolnik GK, Yildiz FH (2000) The complete genome sequence of Vibrio cholerae: a tale of two chromosomes and of two lifestyles. Genome Biol 2000 1:10161011–10161013

    Google Scholar 

  • Seliger SS, Mey AR, Valle A-M, Payne SM (2001) The two TonB systems in Vibrio cholerae: redundant and specific functions. Mol Microbiol 39:801–812

    Article  PubMed  CAS  Google Scholar 

  • Shouldice SR, Dougan DR, Williams PA et al (2003) Crystal structure of Pasteurella haemolytica ferric ion-binding protein A reveals a novel class of bacterial iron-binding proteins. J Biol Chem 278:41093–41098

    Article  PubMed  CAS  Google Scholar 

  • Shouldice SR, Skene RJ, Dougan DR et al (2004) Structural basis for iron binding and release by a novel class of periplasmic iron-binding proteins found in gram-negative pathogens. J Bacteriol 186:3903–3910

    Article  PubMed  CAS  Google Scholar 

  • Sigel SP, Stoebner JA, Payne SM (1985) Iron-vibriobactin transport system is not required for virulence of Vibrio cholerae. Infect Immun 47:360–362

    PubMed  CAS  Google Scholar 

  • Stock JB, Rauch B, Roseman S (1977) Periplasmic space in Salmonella typhimurium and Escherichia coli. J Biol Chem 252:7850–7861

    PubMed  CAS  Google Scholar 

  • Stoebner JA, Payne SM (1988) Iron-regulated hemolysin production and utilization of heme and hemoglobin by Vibrio cholerae. Infect Immun 56:2891–2895

    PubMed  CAS  Google Scholar 

  • Tashima KT, Carroll PA, Rogers MB, Calderwood SB (1996) Relative importance of three iron-regulated outer membrane proteins for in vivo growth of Vibrio cholerae. Infect Immun 64:1756–1761

    PubMed  CAS  Google Scholar 

  • Taylor RK, Miller VL, Furlong DB, Mekalanos JJ (1987) Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci USA 84:2833–2837

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wyckoff EE, Stoebner JA, Reed KE, Payne SM (1997) Cloning of a Vibrio cholerae vibriobactin gene cluster: identification of genes required for early steps in siderophore biosynthesis. J Bacteriol 179:7055–7062

    PubMed  CAS  Google Scholar 

  • Wyckoff EE, Valle A-M, Smith SL, Payne SM (1999) A multifunctional ABC transporter system from Vibrio cholerae transports vibriobactin and enterobactin. J Bacteriol 181:7588–7596

    PubMed  CAS  Google Scholar 

  • Wyckoff EE, Smith SL, Payne SM (2001) VibD and VibH are required for late steps in vibriobactin biosynthesis in Vibrio cholerae. J Bacteriol 183:1830–1834

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wyckoff EE, Mey AR, Leimback A, Fisher CF, Payne SM (2006) Characterization of ferric and ferrous iron transport systems in Vibrio cholerae. J Bacteriol 188:6515–6523

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto S, Okujo N, Fujita Y et al (1993) Structures of two polyamine-containing catecholate siderophores from Vibrio fluvialis. J Biochem (Tokyo) 113:538–544

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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Acknowledgments

We wish to acknowledge Payne lab members past and present who have contributed to our understanding of iron acquisition in V. cholerae, including, Candye Andrus, Suzanne Barth, Stephanie Craig, Carolyn Fisher, Douglas Henderson, Vanamala Kanukurthy, Deborah Occhino Wrona, Stefan Seliger, Janice Stoebner, and Ana Maria Valle. This work was supported by National Institutes of Health Grant AI50669 and the Foundation for Research.

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  1. Section of Molecular Genetics and Microbiology, University of Texas at Austin, 1 University Station A5000, Austin, TX, 78712, USA

    Elizabeth E. Wyckoff, Alexandra R. Mey & Shelley M. Payne

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  1. Elizabeth E. Wyckoff
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  2. Alexandra R. Mey
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Correspondence to Elizabeth E. Wyckoff.

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Wyckoff, E.E., Mey, A.R. & Payne, S.M. Iron acquisition in Vibrio cholerae . Biometals 20, 405–416 (2007). https://doi.org/10.1007/s10534-006-9073-4

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