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Genetics and environmental regulation of Shigella iron transport systems

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Abstract

Shigella spp. have transport systems for both ferric and ferrous iron. The iron can be taken up as free iron or complexed to a variety of carriers. All Shigella species have both the Feo and Sit systems for acquisition of ferrous iron, and all have at least one siderophore-mediated system for transport of ferric iron. Several of the transport systems, including Sit, Iuc/IutA (aerobactin synthesis and transport), Fec (ferric di-citrate uptake), and Shu (heme transport) are encoded within pathogenicity islands. The presence and the genomic locations of these islands vary considerably among the Shigella species, and even between isolates of the same species. The expression of the iron transport systems is influenced by the concentration of iron and by environmental conditions including the level of oxygen. ArcA and FNR regulate iron transport gene expression as a function of oxygen tension, with the sit and iuc promoters being highly expressed in aerobic conditions, while the feo ferrous iron transporter promoter is most active under anaerobic conditions. The effects of oxygen are also seen in infection of cultured cells by Shigella flexneri; the Sit and Iuc systems support plaque formation under aerobic conditions, whereas Feo allows plaque formation anaerobically.

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References

  • Boulette ML (2007) Shigella flexneri ArcA and FNR regulate iron acquisition and contribute to plaque formation under anaerobic conditions. Dissertation, University of Texas, Austin, TX

  • Boulette ML, Payne SM (2007) Anaerobic regulation of Shigella flexneri virulence: ArcA regulates Fur and iron acquisition genes. J Bacteriol 189:6957–6967. doi:10.1128/JB.00621-07

    Article  PubMed  CAS  Google Scholar 

  • Darling AE, Treangen TJ, Messeguer X, Perna NT (2007) Analyzing patterns of microbial evolution using the mauve genome alignment system. Methods Mol Biol 396:135–152. doi:10.1007/978-1-59745-515-2_10

    Article  PubMed  CAS  Google Scholar 

  • Glasner JD, Plunkett GIII, Anderson BD, Baumler DJ, Biehl BS, Burland V, Cabot EL, Darling AE, Mau B, Neeno-Eckwall EC, Pot D, Qiu Y, Rissman AI, Worzella S, Zaremba S, Fedorko J, Hampton T, Liss P, Rusch M, Shaker M, Shaull L, Shetty P, Thotakura S, Whitmore J, Blattner FR, Greene JM, Perna NT (2008) Enteropathogen Resource Integration Center (ERIC): bioinformatics support for research on biodefense-relevant enterobacteria. Nucleic Acids Res 36:D519–D523. doi:10.1093/nar/gkm973

    Article  PubMed  CAS  Google Scholar 

  • Hantke K, Nicholson G, Rabsch W, Winkelmann G (2003) Salmochelins, siderophores of Salmonella enterica and uropathogenic Escherichia coli strains, are recognized by the outer membrane receptor IroN. Proc Natl Acad Sci USA 100:3677–3682. doi:10.1073/pnas.0737682100

    Article  PubMed  CAS  Google Scholar 

  • Headley V, Hong M, Galko M, Payne SM (1997) Expression of aerobactin genes by Shigella flexneri during extracellular and intracellular growth. Infect Immun 65:818–821

    PubMed  CAS  Google Scholar 

  • Janakiraman A, Slauch JM (2000) The putative iron transport system SitABCD encoded on SPI1 is required for full virulence of Salmonella typhimurium. Mol Microbiol 35:1146–1155. doi:10.1046/j.1365-2958.2000.01783.x

    Article  PubMed  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 

  • 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. doi:10.1128/JB.184.12.3159-3166.2002

    Article  PubMed  CAS  Google Scholar 

  • Lawlor KM, Payne SM (1984) Aerobactin genes in Shigella spp. J Bacteriol 160:266–272

    PubMed  CAS  Google Scholar 

  • Lawlor KM, Daskaleros PA, Robinson RE, Payne SM (1987) Virulence of iron transport mutants of Shigella flexneri and utilization of host iron compounds. Infect Immun 55:594–599

    PubMed  CAS  Google Scholar 

  • Lucchini S, Liu H, Jin Q, Hinton JC, Yu J (2005) Transcriptional adaptation of Shigella flexneri during infection of macrophages and epithelial cells: insights into the strategies of a cytosolic bacterial pathogen. Infect Immun 73:88–102. doi:10.1128/IAI.73.1.88-102.2005

    Article  PubMed  CAS  Google Scholar 

  • Luck SN, Turner SA, Rajakumar K, Sakellaris H, Adler B (2001) Ferric dicitrate transport system (Fec) of Shigella flexneri 2a YSH6000 is encoded on a novel pathogenicity island carrying multiple antibiotic resistance genes. Infect Immun 69:6012–6021. doi:10.1128/IAI.69.10.6012-6021.2001

    Article  PubMed  CAS  Google Scholar 

  • Mills M, Payne SM (1997) Identification of shuA, the gene encoding the heme receptor of Shigella dysenteriae, and analysis of invasion and intracellular multiplication of a shuA mutant. Infect Immun 65:5358–5363

    PubMed  CAS  Google Scholar 

  • Moss JE, Cardozo TJ, Zychlinsky A, Groisman EA (1999) The selC-associated SHI-2 pathogenicity island of Shigella flexneri. Mol Microbiol 33:74–83. doi:10.1046/j.1365-2958.1999.01449.x

    Article  PubMed  CAS  Google Scholar 

  • Murphy ER, Payne SM (2007) RyhB, an iron-responsive small RNA molecule, regulates Shigella dysenteriae virulence. Infect Immun 75:3470–3477. doi:10.1128/IAI.00112-07

    Article  PubMed  CAS  Google Scholar 

  • Nassif X, Mazert MC, Mounier J, Sansonetti PJ (1987) Evaluation with an iuc:Tn10 mutant of the role of aerobactin production in the virulence of Shigella flexneri. Infect Immun 55:1963–1969

    PubMed  CAS  Google Scholar 

  • Neilands JB (1984) Siderophores of bacteria and fungi. Microbiol Sci 1:9–14

    PubMed  CAS  Google Scholar 

  • Payne SM (1980) Synthesis and utilization of siderophores by Shigella flexneri. J Bacteriol 143:1420–1424

    PubMed  CAS  Google Scholar 

  • Payne SM, Niesel DW, Peixotto SS, Lawlor KM (1983) Expression of hydroxamate and phenolate siderophores by Shigella flexneri. J Bacteriol 155:949–955

    PubMed  CAS  Google Scholar 

  • Payne SM, Wyckoff EE, Murphy ER, Oglesby AG, Boulette ML, Davies NM (2006) Iron and pathogenesis of Shigella: iron acquisition in the intracellular environment. Biometals 19:173–180. doi:10.1007/s10534-005-4577-x

    Article  PubMed  CAS  Google Scholar 

  • Perry RD, San Clemente CL (1979) Siderophore synthesis in Klebsiella pneumoniae and Shigella sonnei during iron deficiency. J Bacteriol 140:1129–1132

    PubMed  CAS  Google Scholar 

  • Purdy GE, Payne SM (2001) The SHI-3 iron transport island of Shigella boydii 0-1392 carries the genes for aerobactin synthesis and transport. J Bacteriol 183:4176–4182. doi:10.1128/JB.183.14.4176-4182.2001

    Article  PubMed  CAS  Google Scholar 

  • Reeves SA (2001) Iron acquisition in the intracellular environment of the host: multiple iron transport systems in Shigella dysenteriae. Dissertation, University of Texas, Austin, TX

  • Runyen-Janecky LJ, Payne SM (2002) Identification of chromosomal Shigella flexneri genes induced by the eukaryotic intracellular environment. Infect Immun 70:4379–4388

    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 iron acquisition in vitro and in cultured cells. Infect Immun 71(4):1919–1928. doi:10.1128/IAI.71.4.1919-1928.2003

    Article  PubMed  CAS  Google Scholar 

  • Sansonetti PJ (2006) Rupture, invasion and inflammatory destruction of the intestinal barrier by Shigella: the yin and yang of innate immunity. Can J Infect Dis Med Microbiol 17:117–119

    PubMed  Google Scholar 

  • Schmitt MP, Payne SM (1988) Genetics and regulation of enterobactin genes in Shigella flexneri. J Bacteriol 170:5579–5587

    PubMed  CAS  Google Scholar 

  • Schmitt MP, Payne SM (1991) Genetic analysis of the enterobactin gene cluster in Shigella flexneri. J Bacteriol 173:816–825

    PubMed  CAS  Google Scholar 

  • Torres AG, Payne SM (1997) Haem iron-transport system in enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 23:825–833. doi:10.1046/j.1365-2958.1997.2641628.x

    Article  PubMed  CAS  Google Scholar 

  • Vokes SA, Reeves SA, Torres AG, Payne SM (1999) The aerobactin iron transport system genes in Shigella flexneri are present within a pathogenicity island. Mol Microbiol 33:63–73. doi:10.1046/j.1365-2958.1999.01448.x

    Article  PubMed  CAS  Google Scholar 

  • Wei J, Goldberg MB, Burland V, Venkatesan MM, Deng W, Fournier G, Mayhew GF, Plunkett GIII, Rose DJ, Darling A, Mau B, Perna NT, Payne SM, Runyen-Janecky LJ, Zhou S, Schwartz DC, Blattner FR (2003) Complete genome sequence and comparative genomics of Shigella flexneri serotype 2a strain 2457T. Infect Immun 71:2775–2786. doi:10.1128/IAI.71.5.2775-2786.2003

    Article  PubMed  CAS  Google Scholar 

  • Wyckoff EE, Duncan D, Torres AG, Mills M, Maase K, Payne SM (1998) Structure of the Shigella dysenteriae haem transport locus and its phylogenetic distribution in enteric bacteria. Mol Microbiol 28:1139–1152. doi:10.1046/j.1365-2958.1998.00873.x

    Article  PubMed  CAS  Google Scholar 

  • 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. doi:10.1128/JB.187.16.5658-5664.2005

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Yang J, Zhang X, Chen L, Jiang Y, Yan Y, Tang X, Wang J, Xiong Z, Dong J, Xue Y, Zhu Y, Xu X, Sun L, Chen S, Nie H, Peng J, Xu J, Wang Y, Yuan Z, Wen Y, Yao Z, Shen Y, Qiang B, Hou Y, Yu J, Jin Q (2005) Genome dynamics and diversity of Shigella species, the etiologic agents of bacillary dysentery. Nucleic Acids Res 33:6445–6458. doi:10.1093/nar/gki954

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grant AI16935 from the National Institute of Allergy and Infectious Diseases. We thank Alexandra Mey for helpful discussions and critical reading of the manuscript.

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Correspondence to Shelley M. Payne.

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Wyckoff, E.E., Boulette, M.L. & Payne, S.M. Genetics and environmental regulation of Shigella iron transport systems. Biometals 22, 43–51 (2009). https://doi.org/10.1007/s10534-008-9188-x

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