1887

Abstract

The authors previously reported that interspecific stimulatory events between species for antibiotic production and/or morphological differentiation mediated by putative diffusible metabolites take place at a high frequency. This paper reports the isolation and characterization of a substance produced by that stimulates the growth and development of . The substance was purified from the culture supernatant of by using anion-exchange chromatography, gel filtration chromatography and reverse-phase HPLC. FAB-MS and NMR analyses of the purified preparation indicated the substance to be desferrioxamine E (synonym: nocardamine), a siderophore that is widely produced by species and related organisms. Similar stimulatory effects on the growth and development of were exerted by desferrioxamine E produced by another actinomycete strain, but not by other siderophores tested, including ferrichrome and nocobactin and free ferric ion. An exogenous supply of desferrioxamine E stimulated secondary metabolite formation and/or morphological differentiation in various actinomycete strains. Disruption of the desferrioxamine biosynthesis gene cluster in A3(2) abolished the production of desferrioxamine E and the activity to stimulate the growth and differentiation of . The mutant showed impaired growth and development on Bennett's/glucose agar medium, but it was rescued by the exogenous supply of desferrioxamine E. These results indicate that desferrioxamines play an important role in streptomycete physiology. Similar to several pathogenic bacteria and fungi, may be defective in the production of siderophores; however, it can utilize the siderophores excreted by other organisms.

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2005-09-01
2024-10-10
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References

  1. Barona-Gomez 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. Beck E., Ludwig G., Auerswald E. A., Reiss B., Schaller H. 1982; Nucleotide sequence and exact localization of the neomycin phosphotransferase gene from transposon Tn 5. Gene 19:327–336 [CrossRef]
    [Google Scholar]
  3. 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]
  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. Challis G. L., Ravel J. 2000; Coelichelin, a new peptide siderophore encoded by the Streptomyces coelicolor genome: structure prediction from the sequence of its non-ribosomal peptide synthetase. FEMS Microbiol Lett 187:111–114 [CrossRef]
    [Google Scholar]
  6. Chater K. F. 1993; Genetics of differentiation in Streptomyces . Annu Rev Microbiol 47:685–713 [CrossRef]
    [Google Scholar]
  7. Horinouchi S. 1999; Gamma-butyrolactones that control secondary metabolism and cell differentiation in Streptomyces . In Cell–Cell Signaling in Bacteria pp 193–207 Edited by Dunny G. M., Winans S. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  8. Horinouchi S. 2002; A microbial hormone, A-factor, as a master switch for morphological differentiation and secondary metabolism in Streptomyces griseus . Front Biosci 7:2045–2057 [CrossRef]
    [Google Scholar]
  9. Horinouchi S., Beppu T. 1992; Autoregulatory factors and communication in actinomycetes. Annu Rev Microbiol 46:377–398 [CrossRef]
    [Google Scholar]
  10. Horinouchi S., Kumada Y., Beppu T. 1984; Unstable genetic determinant of A-factor biosynthesis in streptomycin-producing organisms: cloning and characterization. J Bacteriol 158:481–487
    [Google Scholar]
  11. Kieser T., Bibb M. J., Buttner M. J., Chater K. F., Hopwood D. A. 2000 Practical Streptomyces Genetics Norwich, UK: John Innes Foundation;
    [Google Scholar]
  12. Kingsley R. A., Reissbrodt R., Rabsch W. 7 other authors 1999; Ferrioxamine-mediated iron(III) utilization by Salmonella enterica . Appl Environ Microbiol 65:1610–1618
    [Google Scholar]
  13. Lesuisse E., Blaiseau P. L., Dancis A., Camadro J. M. 2001; Siderophore uptake and use by the yeast Saccharomyces cerevisiae . Microbiology 147:289–298
    [Google Scholar]
  14. Maniatis T., Fritsch E. F., Sambrook J. 1982 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  15. Matsubara K., Sakuda S., Kondo T., Tanaka M., Nishimura T., Suzuki A. 1998; Morphological changes in insect BM-N4 cells induced by nocardamine. Biosci Biotechnol Biochem 62:2049–2051 [CrossRef]
    [Google Scholar]
  16. Meyer J. M., Abdallah M. A. 1980; The siderochromes of nonfluorescent Pseudomonas : production of nocardamine by Pseudomonas stutzeri . J Gen Microbiol 118:125–129
    [Google Scholar]
  17. Miyadoh S. 1993; Research on antibiotic screening in Japan over the last decade: a producing microorganisms approach. Actinomycetologica 7:100–106 [CrossRef]
    [Google Scholar]
  18. Müller G., Raymond K. N. 1984; Specificity and mechanism of ferrioxamine-mediated iron transport in Streptomyces pilosus . J Bacteriol 160:304–312
    [Google Scholar]
  19. Müller G., Matzanke B. F., Raymond K. N. 1984; Iron transport in Streptomyces pilosus mediated by ferrichrome siderophores, rhodotorulic acid, and enantio-rhodotorulic acid. J Bacteriol 160:313–318
    [Google Scholar]
  20. Prelog V. 1963; Iron containing antibiotics and microbic growth factors. Pure Appl Chem 6:327–338
    [Google Scholar]
  21. Schryvers A. B., Stojiljkovic I. 1999; Iron acquisition systems in the pathogenic Neisseria. Mol Microbiol 32:1117–1123 [CrossRef]
    [Google Scholar]
  22. 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]
  23. Schwyn B., Neilands J. B. 1987; Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56 [CrossRef]
    [Google Scholar]
  24. Takano E., Nihira T., Hara Y., Jones J. J., Gershater C. J., Yamada Y., Bibb M. 2000; Purification and structural determination of SCB1, a gamma-butyrolactone that elicits antibiotic production in Streptomyces coelicolor A3(2. J Biol Chem 275:11010–11016 [CrossRef]
    [Google Scholar]
  25. Tam T. F., Leung-Toung R., Li W., Wang Y., Karimian K., Spino M. 2003; Iron chelator research: past, present, and future. Curr Med Chem 10:983–995 [CrossRef]
    [Google Scholar]
  26. Ueda K., Kawai S., Ogawa H., Kiyama A., Kubota T., Kawanobe H., Beppu T. 2000; Wide distribution of interspecific stimulatory events on antibiotic production and sporulation among Streptomyces species. J Antibiot 53:979–982 [CrossRef]
    [Google Scholar]
  27. Yamada Y. 1999; Autoregulatory factors and regulation of antibiotic production in Streptomyces . In Microbial Signalling and Communication pp 177–196 Edited by England R. R., Hobbs G., Bainton N. J., Roberts D. M. Cambridge: Cambridge University Press;
    [Google Scholar]
  28. Yun C. W., Ferea T., Rashford J., Ardon O., Brown P. O., Botstein D., Kaplan J., Philpott C. C. 2000; Desferrioxamine-mediated iron uptake in Saccharomyces cerevisiae . Evidence for two pathways of iron uptake. J Biol Chem 275:10709–10715 [CrossRef]
    [Google Scholar]
  29. Zahner H., Bachmann E., Hutter R., Nuesch J. 1962; Sideramine, eisenhaltige Wachstumsfaktoren aus Mikroorganismen. Pathol Microbiol 25:708–736
    [Google Scholar]
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