1887

Abstract

Siderophore-mediated iron acquisition has been well studied in many bacterial pathogens because it contributes to virulence. In contrast, siderophore-mediated iron acquisition by saprophytic bacteria has received relatively little attention. The independent identification of the and gene clusters that direct production of the -hydroxamate ferric iron-chelators desferrioxamine E and coelichelin, respectively, which could potentially act as siderophores in the saprophyte A3(2), has recently been reported. Here it is shown that the cluster also directs production of desferrioxamine B in and that very similar and clusters direct production of desferrioxamines E and B, and coelichelin, respectively, in s ATCC 23877. Sequence analyses of the and clusters suggest that components of ferric-siderophore uptake systems are also encoded within each cluster. The construction and analysis of a series of mutants of lacking just biosynthetic genes or both the biosynthetic and siderophore uptake genes from the and clusters demonstrated that coelichelin and desferrioxamines E and B all function as siderophores in this organism and that at least one of these metabolites is required for growth under defined conditions even in the presence of significant quantities of ferric iron. These experiments also demonstrated that a third siderophore uptake system must be present in , in addition to the two encoded within the and clusters, which show selectivity for coelichelin and desferrioxamine E, respectively. The ability of the mutants to utilize a range of exogenous xenosiderophores for iron acquisition was also examined, showing that the third siderophore-iron transport system has broad specificity for -hydroxamate-containing siderophores. Together, these results define a complex system of multiple biosynthetic and uptake pathways for siderophore-mediated iron acquisition in and .

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2006-11-01
2024-03-28
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References

  1. Barona-Gómez F, Wong U, Giannakopulos A. E, Derrick P. J, Challis G. L. 2004; Identification of a cluster of genes that directs desferrioxamine biosynthesis in Streptomyces coelicolor M145. J Am Chem Soc 126:16282–16283 [CrossRef]
    [Google Scholar]
  2. Bentley S. D, Chater K. F, Cerdeno-Tarraga A. M. 40 other authors 2002; Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147 [CrossRef]
    [Google Scholar]
  3. 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]
  4. Bickel H, Bosshardt R, Gaumann E, Reusser P, Vischer E, Voser W, Wettstein A, Zahner H. 1960; Metabolic products of Actinomycetaceae. XXVI. Isolation and properties of ferrioxamines A to F, representing new sideramine compounds. Helv Chim Acta 43:2118–2128 [CrossRef]
    [Google Scholar]
  5. Blondelet-Rouault M. H, Weiser J, Lebrihi A, Branny P, Pernodet J. L. 1997; Antibiotic resistance gene cassettes derived from the omega interposon for use in E. coli and Streptomyces . Gene 190:315–317 [CrossRef]
    [Google Scholar]
  6. Bunet R, Brock A, Rexer H.-U, Takano E. 2006; Identification of genes involved in siderophore transport in Streptomyces coelicolor A3(2). FEMS Microbiol Lett 262:57–64 [CrossRef]
    [Google Scholar]
  7. Butterton J. R, Calderwood S. B. 1994; Identification, cloning, and sequencing of a gene required for ferric vibriobactin utilization by Vibrio cholerae . J Bacteriol 176:5631–5638
    [Google Scholar]
  8. Cendrowski S, MacArthur W, Hanna P. 2004; Bacillus anthracis requires siderophore biosynthesis for growth in macrophages and mouse virulence. Mol Microbiol 51:407–417 [CrossRef]
    [Google Scholar]
  9. Challis G. L. 2005; A widely distributed bacterial pathway for siderophore biosynthesis independent of nonribosomal peptide synthetases. Chembiochem 6:601–611 [CrossRef]
    [Google Scholar]
  10. Challis G. L, Hopwood D. A. 2003; Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci U S A 100:14555–14561 [CrossRef]
    [Google Scholar]
  11. Challis G. L, Naismith J. H. 2004; Structural aspects of non-ribosomal peptide biosynthesis. Curr Opin Struct Biol 14:748–756 [CrossRef]
    [Google Scholar]
  12. Chipperfield J. R, Ratledge C. 2000; Salicylic acid is not a bacterial siderophore: a theoretical study. Biometals 13:165–168 [CrossRef]
    [Google Scholar]
  13. Choulet F, Aigle B, Gallois A. 9 other authors 2006; Evolution of the terminal regions of the Streptomyces linear chromosome. Mol Biol Evol (in press)
    [Google Scholar]
  14. Crosa J. H, Walsh C. T. 2002; Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev 66:223–249 [CrossRef]
    [Google Scholar]
  15. Crosa J. H, Mey A. R, Payne S. M. 2004 Iron Transport in Bacteria Washington: ASM Press;
    [Google Scholar]
  16. Fath M. J, Kolter R. 1993; ABC transporters: bacterial exporters. Microbiol Rev 57:995–1017
    [Google Scholar]
  17. Flores F. J, Martín J. F. 2004; Iron-regulatory proteins DmdR1 and DmdR2 of Streptomyces coelicolor form two different DNA–protein complexes with iron boxes. Biochem J 380:497–503 [CrossRef]
    [Google Scholar]
  18. Franza T, Mahe B, Expert D. 2005; Erwinia chrysanthemi requires a second iron transport route dependent of the siderophore achromobactin for extracellular growth and plant infection. Mol Microbiol 55:261–275
    [Google Scholar]
  19. Günter-Seeboth K., Schupp T. 1995; Cloning and sequence analysis of the Corynebacterium diptheriae dtxR homologue from Streptomyces lividans and Streptomyces pilosus encoding a putative iron repressor protein. Gene 166:117–119 [CrossRef]
    [Google Scholar]
  20. Günter K, Toupet C, Schupp T. 1993; Characterisation of an iron-regulated promoter involved in deferrioxamine B synthesis in Streptomyces pilosus : repressor binding site and homology to the diphtheria toxin gene promoter. J Bacteriol 175:3295–3302
    [Google Scholar]
  21. Gust B, Challis G. L, Fowler K, Kieser T, Chater K. F. 2003; PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci U S A 100:1541–1546 [CrossRef]
    [Google Scholar]
  22. Hood D. W, Heidstra R, Swoboda U. K, Hodgson D. A. 1992; Molecular genetic analysis of proline and tryptophan biosynthesis in Streptomyces coelicolor A3(2): interaction between primary and secondary metabolism – a review. Gene 115:5–12 [CrossRef]
    [Google Scholar]
  23. Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Omura S. 2003; Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis . Nat Biotechnol 21:526–531 [CrossRef]
    [Google Scholar]
  24. Imbert M, Blondeau R, Béchet M. 1995; Comparison of the main siderophores produced by some species of Streptomyces . Curr Microbiol 31:129–133 [CrossRef]
    [Google Scholar]
  25. Kachadourian R, Dellagi A, Laurent J, Bricard L, Kunesch G, Expert D. 1996; Desferrioxamine-dependent iron transport in Erwinia amylovora CFBP1430: cloning of the gene encoding the ferrioxamine receptor FoxR. Biometals 9:143–150
    [Google Scholar]
  26. Kieser T, Bibb M. J, Buttner M. J, Chater K. F, Hopwood D. A. 2000 Practical Streptomyces Genetics Norwich: The John Innes Foundation;
    [Google Scholar]
  27. Kim D.-W, Chater K. F, Lee K.-J, Hesketh A. 2005; Effects of growth phase and the developmentally significant bldA -specified tRNA on the membrane-associated proteome of Streptomyces coelicolor . Microbiology 151:2707–2720 [CrossRef]
    [Google Scholar]
  28. Lautru S, Deeth R. J, Bailey L. M, Challis G. L. 2005; Discovery of a new peptide natural product by Streptomyces coelicolor genome mining. Nat Chem Biol 1:265–269 [CrossRef]
    [Google Scholar]
  29. Mark B. L, Wasney G. A, Salo T. J, Khan A. R, Cao Z, Robbins P. W, James M. N, Triggs-Raine B. L. 1998; Structural and functional characterization of Streptomyces plicatus β - N -acetylhexosaminidase by comparative molecular modeling and site-directed mutagenesis. J Biol Chem 273:19618–19624 [CrossRef]
    [Google Scholar]
  30. 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]
  31. Muller G, Raymond K. N. 1984; Specificity and mechanism of ferrioxamine-mediated iron transport in Streptomyces pilosus . J Bacteriol 160:304–312
    [Google Scholar]
  32. Poole K, McKay G. A. 2003; Iron acquisition and its control in Pseudomonas aeruginosa : many roads lead to Rome. Front Biosci 8:d661–d686 [CrossRef]
    [Google Scholar]
  33. Raynal A, Karray F, Tuphile K, Pernodet J.-L, Darbon-Rongère E. 2006; Excisable cassettes: new tools for functional analysis of Streptomyces genomes. Appl Environ Microbiol 72:4839–4844 [CrossRef]
    [Google Scholar]
  34. Redenbach M, Kieser H. M, Denapaite D, Eichner A, Cullum J, Kinashi H, Hopwood D. A. 1996; A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome. Mol Microbiol 21:77–96 [CrossRef]
    [Google Scholar]
  35. Schneider R, Hantke K. 1993; Iron-hydroxamate uptake systems in Bacillus subtilis : identification of a lipoprotein as part of a binding protein-dependent transport system. Mol Microbiol 8:111–121 [CrossRef]
    [Google Scholar]
  36. Schupp T, Waldmeier U, Divers M. 1987; Biosynthesis of desferrioxamine B in Streptomyces pilosus : evidence for the involvement of lysine decarboxylase. FEMS Microbiol Lett 42:135–139 [CrossRef]
    [Google Scholar]
  37. Schupp T, Toupet C, Divers M. 1988; Cloning and expression of two genes of Streptomyces pilosus involved in the biosynthesis of the siderophore desferrioxamine B. Gene 64:179–188 [CrossRef]
    [Google Scholar]
  38. Sebulsky M. T, Heinrichs D. E. 2001; Identification and characterization of fhuD1 and fhuD2 , two genes involved in iron-hydroxamate uptake in Staphylococcus aureus . J Bacteriol 183:4994–5000 [CrossRef]
    [Google Scholar]
  39. Simon R, Priefer U, Pühler A. 1983; A broad host range mobilisation system for in vivo genetic engineering: transposon mutagenesis in gram-negative bacteria. Biotechnology 1:784–791 [CrossRef]
    [Google Scholar]
  40. Wandersman C, Delepelaire P. 2004; Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647 [CrossRef]
    [Google Scholar]
  41. Winkelmann G, Drechsel H. 1997; Microbial siderophores. In Biotechnology, vol. 7, Products of Secondary Metabolism, 2nd edn. pp  200–246 Edited by Rehm H.-J., Reed G., Kleinkauf H., von-Döhren H. Weinheim: VCH;
    [Google Scholar]
  42. Yamanaka K, Oikawa H, Ogawa H, Hosono K, Shinmachi F, Takano H, Sakuda S, Beppu T, Ueda K. 2005; Desferrioxamine E produced by Streptomyces griseus stimulates growth and development of Streptomyces tanashiensis . Microbiology 151:2899–2905 [CrossRef]
    [Google Scholar]
  43. Yeats C, Bentley S, Bateman A. 2003; New knowledge from old: in silico discovery of novel protein domains in Streptomyces coelicolor . BMC Microbiol 3:3 [CrossRef]
    [Google Scholar]
  44. Zhang Y.-X, Denoya C. D, Skinner D. D. 7 other authors 1999; Genes encoding acyl-CoA dehydrogenase (AcdH) homologues from Streptomyces coelicolor and Streptomyces avermitilis provide insights into the metabolism of small branched-chain fatty acids and macrolide antibiotic production. Microbiology 145:2323–2334
    [Google Scholar]
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