1887

Abstract

The chemolithoautotroph has two genes predicted to encode outer-membrane (OM) ferrioxamine transporters. Expression of the ferrioxamine uptake system required induction, as shown by the shorter lag phase in ferrioxamine-containing cultures when ferrioxamine-exposed cells were used as an inoculum. The two OM ferrioxamine siderophore transporters encoded by (NE1097) and (NE1088) were produced only in cells grown in Fe-limited ferrioxamine-containing medium. The inactivation of , singly or in combination with , prevented growth in Fe-limited medium containing excess desferrioxamine (DFX). The -disrupted single mutant grew poorly in the regular Fe-limited (0.2 μM) medium with 10 μM DFX, but grew well when the Fe level was raised to 1.0 μM with 10 μM DFX. For efficient acquisition of Fe-loaded ferrioxamine, needs both ferrioxamine transporters FoxA and FoxA. FoxA probably regulates its own production, and it controls the production of FoxA as well.

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2007-12-01
2019-10-18
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References

  1. Baumler, A. J. & Hantke, K. ( 1992; ). Ferrioxamine uptake in Yersinia enterocolitica: characterization of the receptor protein FoxA. Mol Microbiol 6, 1309–1321.[CrossRef]
    [Google Scholar]
  2. Bell, K. S., Sebaihia, M., Pritchard, L., Holden, M. T., Hyman, L. J., Holeva, M. C., Thomson, N. R., Bentley, S. D., Churcher, L. J. & other authors ( 2004; ). Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci U S A 101, 11105–11110.[CrossRef]
    [Google Scholar]
  3. Berner, I. & Winkelmann, G. ( 1990; ). Ferrioxamine transport mutants and the identification of the ferrioxamine receptor protein (FoxA) in Erwinia herbicola (Enterobacter agglomerans). Biol Met 2, 197–202.[CrossRef]
    [Google Scholar]
  4. Berner, I., Konetschny-Rapp, S., Jung, G. & Winkelmann, G. ( 1988; ). Characterization of ferrioxamine E as the principal siderophore of Erwinia herbicola (Enterobacter agglomerans). Biol Met 1, 51–56.[CrossRef]
    [Google Scholar]
  5. Berry, E. A. & Trumpower, B. L. ( 1987; ). Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra. Anal Biochem 161, 1–15.[CrossRef]
    [Google Scholar]
  6. Braun, V. ( 1997; ). Surface signaling: novel transcription initiation mechanism starting from the cell surface. Arch Microbiol 167, 325–331.[CrossRef]
    [Google Scholar]
  7. Braun, V. & Killmann, H. ( 1999; ). Bacterial solutions to the iron-supply problem. Trends Biochem Sci 24, 104–109.[CrossRef]
    [Google Scholar]
  8. Braun, V., Mahren, S. & Ogierman, M. ( 2003; ). Regulation of the FecI-type ECF sigma factor by transmembrane signalling. Curr Opin Microbiol 6, 173–180.[CrossRef]
    [Google Scholar]
  9. Carter, P. ( 1971; ). Spectrophotometric determination of serum iron at the submicrogram level with a new reagent (ferrozine). Anal Biochem 40, 450–458.[CrossRef]
    [Google Scholar]
  10. Chain, P., Lamerdin, J., Larimer, F., Regala, W., Lao, V., Land, M., Hauser, L., Hooper, A., Klotz, M. & other authors ( 2003; ). Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J Bacteriol 185, 2759–2773.[CrossRef]
    [Google Scholar]
  11. Champomier-Verges, M. C., Stintzi, A. & Meyer, J. M. ( 1996; ). Acquisition of iron by the non-siderophore-producing Pseudomonas fragi. Microbiology 142, 1191–1199.[CrossRef]
    [Google Scholar]
  12. Chiu, C. H., Tang, P., Chu, C., Hu, S., Bao, Q., Yu, J., Chou, Y. Y., Wang, H. S. & Lee, Y. S. ( 2005; ). The genome sequence of Salmonella enterica serovar Choleraesuis, a highly invasive and resistant zoonotic pathogen. Nucleic Acids Res 33, 1690–1698.[CrossRef]
    [Google Scholar]
  13. Clarke, T. E., Tari, L. W. & Vogel, H. J. ( 2001; ). Structural biology of bacterial iron uptake systems. Curr Top Med Chem 1, 7–30.[CrossRef]
    [Google Scholar]
  14. Deiss, K., Hantke, K. & Winkelmann, G. ( 1998; ). Molecular recognition of siderophores: a study with cloned ferrioxamine receptors (FoxA) from Erwinia herbicola and Yersinia enterocolitica. Biometals 11, 131–137.[CrossRef]
    [Google Scholar]
  15. Ensign, S. A., Hyman, M. R. & Arp, D. J. ( 1993; ). In vitro activation of ammonia monooxygenase from Nitrosomonas europaea by copper. J Bacteriol 175, 1971–1980.
    [Google Scholar]
  16. Escolar, L., Perez-Martin, J. & de Lorenzo, V. ( 1999; ). Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181, 6223–6229.
    [Google Scholar]
  17. Faraldo-Gomez, J. D. & Sansom, M. S. ( 2003; ). Acquisition of siderophores in gram-negative bacteria. Nat Rev Mol Cell Biol 4, 105–116.[CrossRef]
    [Google Scholar]
  18. Gaspar, M., Santos, M. A., Krauter, K. & Winkelmann, G. ( 1999; ). Molecular recognition of synthetic siderophore analogues: a study with receptor-deficient and fhu(A-B) deletion mutants of Escherichia coli. Biometals 12, 209–218.[CrossRef]
    [Google Scholar]
  19. Gunter, K., Toupet, C. & Schupp, T. ( 1993; ). Characterization of an iron-regulated promoter involved in desferrioxamine B synthesis in Streptomyces pilosus: repressor-binding site and homology to the diphtheria toxin gene promoter. J Bacteriol 175, 3295–3302.
    [Google Scholar]
  20. Hageman, R. H. & Hucklesby, D. P. ( 1971; ). Nitrate reductase in higher plants. Methods Enzymol 23, 491–503.
    [Google Scholar]
  21. Hoegy, F., Celia, H., Mislin, G. L., Vincent, M., Gallay, J. & Schalk, I. J. ( 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.[CrossRef]
    [Google Scholar]
  22. Hommes, N. G., Sayavedra-Soto, L. A. & Arp, D. J. ( 1996; ). Mutagenesis of hydroxylamine oxidoreductase in Nitrosomonas europaea by transformation and recombination. J Bacteriol 178, 3710–3714.
    [Google Scholar]
  23. Hooper, A. B., Erickson, R. H. & Terry, K. R. ( 1972; ). Electron transport systems of Nitrosomonas: isolation of a membrane-envelope fraction. J Bacteriol 110, 430–438.
    [Google Scholar]
  24. Houk, R. S. ( 1994; ). Elemental and isotopic analysis by inductively coupled plasma mass spectrometry. Acc Chem Res 27, 333–339.[CrossRef]
    [Google Scholar]
  25. Hyman, M. R. & Arp, D. J. ( 1993; ). An electrophoretic study of the thermal-dependent and reductant-dependent aggregation of the 27 kDa component of ammonia monooxygenase from Nitrosomonas europaea. Electrophoresis 14, 619–627.[CrossRef]
    [Google Scholar]
  26. Killmann, H. & Braun, V. ( 1998; ). Conversion of the coprogen transport protein FhuE and the ferrioxamine B transport protein FoxA into ferrichrome transport proteins. FEMS Microbiol Lett 161, 59–67.[CrossRef]
    [Google Scholar]
  27. 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.[CrossRef]
    [Google Scholar]
  28. Kingsley, R. A., Reissbrodt, R., Rabsch, W., Ketley, J. M., Tsolis, R. M., Everest, P., Dougan, G., Bäumler, A. J., Roberts, M. & Williams, P. H. ( 1999; ). Ferrioxamine-mediated iron(III) utilization by Salmonella enterica. Appl Environ Microbiol 65, 1610–1618.
    [Google Scholar]
  29. Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M., II & Peterson, K. M. ( 1995; ). Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166, 175–176.[CrossRef]
    [Google Scholar]
  30. Livak, K. J. & Schmittgen, T. D. ( 2001; ). Analysis of relative gene expression data using real-time quantitative PCR and the <-- INSERT PICT -->method. Methods 25, 402–408.[CrossRef]
    [Google Scholar]
  31. Llamas, M. A., Sparrius, M., Kloet, R., Jimenez, C. R., Vandenbroucke-Grauls, C. & Bitter, W. ( 2006; ). The heterologous siderophores ferrioxamine B and ferrichrome activate signaling pathways in Pseudomonas aeruginosa. J Bacteriol 188, 1882–1891.[CrossRef]
    [Google Scholar]
  32. Mahren, S. & Braun, V. ( 2003; ). The FecI extracytoplasmic-function sigma factor of Escherichia coli interacts with the β′ subunit of RNA polymerase. J Bacteriol 185, 1796–1802.[CrossRef]
    [Google Scholar]
  33. 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.[CrossRef]
    [Google Scholar]
  34. Meyer, J.-M. ( 1992; ). Exogenous siderophore-mediated iron uptake in Pseudomonas aeruginosa: possible involvement of porin OprF in iron translocation. J Gen Microbiol 138, 951–958.[CrossRef]
    [Google Scholar]
  35. Meyer, J.-M. & Abdallah, M. A. ( 1980; ). The siderochromes of non-fluorescent pseudomonads: production of nocardamine by Pseudomonas stutzeri. J Gen Microbiol 118, 125–129.
    [Google Scholar]
  36. Muller, G. & Raymond, K. N. ( 1984; ). Specificity and mechanism of ferrioxamine-mediated iron transport in Streptomyces pilosus. J Bacteriol 160, 304–312.
    [Google Scholar]
  37. Neilands, J. B. ( 1995; ). Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270, 26723–26726.[CrossRef]
    [Google Scholar]
  38. Pfaffl, M. W. ( 2001; ). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, e45 [CrossRef]
    [Google Scholar]
  39. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  40. Schalk, I. J., Hennard, C., Dugave, C., Poole, K., Abdallah, M. A. & Pattus, F. ( 2001; ). Iron-free pyoverdin binds to its outer membrane receptor FpvA in Pseudomonas aeruginosa: a new mechanism for membrane iron transport. Mol Microbiol 39, 351–360.[CrossRef]
    [Google Scholar]
  41. Schalk, I. J., Yue, W. W. & Buchanan, S. K. ( 2004; ). Recognition of iron-free siderophores by TonB-dependent iron transporters. Mol Microbiol 54, 14–22.[CrossRef]
    [Google Scholar]
  42. Schweizer, H. D. ( 1993; ). Small broad-host-range gentamicin resistance gene cassettes for site-specific insertion and deletion mutagenesis. Biotechniques 15, 831–834.
    [Google Scholar]
  43. Stein, L. Y. & Arp, D. J. ( 1998; ). Loss of ammonia monooxygenase activity in Nitrosomonas europaea upon exposure to nitrite. Appl Environ Microbiol 64, 4098–4102.
    [Google Scholar]
  44. Stintzi, A., Barnes, C., Xu, J. & Raymond, K. N. ( 2000; ). Microbial iron transport via a siderophore shuttle: a membrane ion transport paradigm. Proc Natl Acad Sci U S A 97, 10691–10696.[CrossRef]
    [Google Scholar]
  45. Visca, P., Leoni, L., Wilson, M. J. & Lamont, I. L. ( 2002; ). Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol Microbiol 45, 1177–1190.[CrossRef]
    [Google Scholar]
  46. Wei, X., Sayavedra-Soto, L. A. & Arp, D. J. ( 2004; ). The transcription of the cbb operon in Nitrosomonas europaea. Microbiology 150, 1869–1879.[CrossRef]
    [Google Scholar]
  47. Wei, X., Vajrala, N., Hauser, L., Sayavedra-Soto, L. A. & Arp, D. J. ( 2006; ). Iron nutrition and physiological responses to iron stress in Nitrosomonas europaea. Arch Microbiol 186, 107–118.[CrossRef]
    [Google Scholar]
  48. Winkelmann, G. ( 1991; ). Specificity of iron transport in bacteria and fungi. In CRC Handbook of Microbial Iron Chelates, pp. 366. Edited by G. Winkelmann. Boca Raton, FL: CRC Press.
  49. Yue, W. W., Grizot, S. & Buchanan, S. K. ( 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.[CrossRef]
    [Google Scholar]
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