1887

Abstract

Proferrorosamine A (proFRA) is an iron (Fe) chelator produced by the opportunistic plant pathogen P45. To identify genes involved in proFRA synthesis, transposon mutagenesis was performed. The identified 9.3 kb gene cluster, comprising seven genes, designated , encodes proteins that are involved in proFRA synthesis. Based on gene homologies, a biosynthetic pathway model for proFRA is proposed. To obtain a better understanding of the effect of proFRA on non-proFRA producing bacteria, P45 was co-cultured with CFBP1430, a fire-blight-causing plant pathogen. P45, but not corresponding proFRA-negative mutants, led to a pink coloration of CFBP1430 colonies on King's B agar, indicating accumulation of the proFRA–iron complex ferrorosamine, and growth inhibition . By saturating proFRA-containing extracts with Fe, the inhibitory effect was neutralized, suggesting that the iron-chelating capability of proFRA is responsible for the growth inhibition of CFBP1430.

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2016-02-01
2024-03-28
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References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [View Article][PubMed]
    [Google Scholar]
  2. Badarinarayana V., Estep P. W. III, Shendure J., Edwards J., Tavazoie S., Lam F., Church G. M. 2001; Selection analyses of insertional mutants using subgenic-resolution arrays. Nat Biotechnol 19:1060–1065 [View Article][PubMed]
    [Google Scholar]
  3. Brady C., Cleenwerck I., Venter S., Vancanneyt M., Swings J., Coutinho T. 2008; Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst Appl Microbiol 31:447–460 [View Article][PubMed]
    [Google Scholar]
  4. Carrell C. J., Bruckner R. C., Venci D., Zhao G., Jorns M. S., Mathews F. S. 2007; NikD, an unusual amino acid oxidase essential for nikkomycin biosynthesis: structures of closed and open forms at 1.15 and 1.90 Å resolution. Structure 15:928–941 [View Article][PubMed]
    [Google Scholar]
  5. Chiou C. S., Jones A. L. 1995; Molecular analysis of high-level streptomycin resistance in Erwinia amylovora . Phytopathology 85:324–328 [View Article]
    [Google Scholar]
  6. De Vos P., Vande Woestyne M., Vancanneyt M., Verstraete W., Kersters K. 1993; Identification of proferrorosamine producing Pseudomonas sp. strain GH (LMG 11358) as Erwinia rhapontici . Syst Appl Microbiol 16:252–255 [View Article]
    [Google Scholar]
  7. Dellagi A., Brisset M. N., Paulin J. P., Expert D. 1998; Dual role of desferrioxamine in Erwinia amylovora pathogenicity. Mol Plant Microbe Interact 11:734–742 [View Article][PubMed]
    [Google Scholar]
  8. Earhart C. F. 1996; Uptake and metabolism of iron and molybdenum. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp 1075–1090 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  9. EPPO 2013; Erwinia amylovora . Bull OEPP/EPPO 43:21–45 [CrossRef]
    [Google Scholar]
  10. Feistner G., Korth H., Ko H., Pulverer G., Budzikiewicz H. 1983; Ferrorosamine A from Erwinia rhapontici . Curr Microbiol 8:239–243 [View Article]
    [Google Scholar]
  11. Feistner G. J., Stahl D. C., Gabrik A. H. 1993; Proferrioxamine siderophores of Erwinia amylovora – a capillary liquid-chromatographic electrospray tandem mass-spectrometric study. Org Mass Spectrom 28:163–175 [View Article]
    [Google Scholar]
  12. Feistner G. J., Mavridis A., Rudolph K. 1997; Proferrorosamines and phytopathogenicity in Erwinia spp. Biometals 10:1–10 [View Article][PubMed]
    [Google Scholar]
  13. Galán J. E., Ginocchio C., Costeas P. 1992; Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J Bacteriol 174:4338–4349[PubMed]
    [Google Scholar]
  14. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580 [View Article][PubMed]
    [Google Scholar]
  15. Holenstein G. 2011 A putative Bradyrhizobium japonicum metalloprotease: highly conserved, largely enigmatic. PhD thesis, Eidgenösschische Technische Hochschule, Zürich, Switzerland
  16. Johnson K. B., Temple T. N. 2013; Evaluation of strategies for fire blight control in organic pome fruit without antibiotics. Plant Dis 97:402–409 [View Article]
    [Google Scholar]
  17. 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 [View Article][PubMed]
    [Google Scholar]
  18. Kamber T., Smits T. H. M., Duffy B. 2012; Genomics of the fire blight pathogen Erwinia and control agent Pantoea . Trees 26:227–238 [View Article]
    [Google Scholar]
  19. Lagendijk E. L., Validov S., Lamers G. E., de Weert S., Bloemberg G. V. 2010; Genetic tools for tagging Gram-negative bacteria with mCherry for visualization in vitro and in natural habitats, biofilm and pathogenicity studies. FEMS Microbiol Lett 305:81–90 [View Article][PubMed]
    [Google Scholar]
  20. Liu W. C., Fisher S. M., Wells J.S., Jr, Ricca C. S., Principe P. A., Trejo W. H., Bonner D. P., Gougoutos J. Z., Toeplitz B. K., Sykes R. B. 1981; Siderochelin, a new ferrous-ion chelating agent produced by Nocardia . J Antibiot (Tokyo) 34:791–799 [View Article][PubMed]
    [Google Scholar]
  21. Loper J. E., Henkels M. D., Roberts R. G., Grove G. G., Willet T. J., Smith T. J. 1991; Evaluation of streptomycin and oxytetracycline and copper resistance of Erwinia amylovora isolated from pear orchards in Washington State. Plant Dis 75:287–290 [View Article]
    [Google Scholar]
  22. Lu C. H., Ye F. W., Shen Y. M. 2015; Siderochelins with anti-mycobacterial activity from Amycolatopsis sp. LZ149. Chin J Nat Med 13:69–72[PubMed] [CrossRef]
    [Google Scholar]
  23. Manulis S., Kleitman F., Shtienberg D., Shwartz H., Oppenheim D., Zilberstaine M., Shabi E. 2003; Changes in the sensitivity of Erwinia amylovora populations to streptomycin and oxolinic acid in Israel. Plant Dis 87:650–654 [View Article]
    [Google Scholar]
  24. McGhee G. C., Sundin G. W. 2011; Evaluation of kasugamycin for fire blight management, effect on nontarget bacteria, and assessment of kasugamycin resistance potential in Erwinia amylovora . Phytopathology 101:192–204 [View Article][PubMed]
    [Google Scholar]
  25. McManus P. S. 2014; Does a drop in the bucket make a splash? Assessing the impact of antibiotic use on plants. Curr Opin Microbiol 19:76–82 [View Article][PubMed]
    [Google Scholar]
  26. McManus P. S., Stockwell V. O., Sundin G. W., Jones A. L. 2002; Antibiotic use in plant agriculture. Annu Rev Phytopathol 40:443–465 [View Article][PubMed]
    [Google Scholar]
  27. Miller V. L., Mekalanos J. J. 1988; A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR . J Bacteriol 170:2575–2583[PubMed]
    [Google Scholar]
  28. Mitscher L. A., Högberg T., Drake S. D., Burgstahler A. W., Jackson M., Lee B., Sheldon R. I., Gracey H. E., Kohl W., Theriault R. J. 1984; Isolation and structural determination of siderochelin C, a fermentation product of an unusual Actinomycetes sp. J Antibiot (Tokyo) 37:1260–1263 [View Article][PubMed]
    [Google Scholar]
  29. Paulin J. P., Samson R. 1973; [Fire blight in France: II. Characters of the strains of Erwinia amylovora (Burril) Winslow et al., 1920, isolated from a Franco-Belgian focus]. Annu Phytopathol 5:389–397 (in French)
    [Google Scholar]
  30. Piqué N., Miñana-Galbis D., Merino S., Tomás J. M. 2015; Virulence factors of Erwinia amylovora: a review. Int J Mol Sci 16:12836–12854 [View Article][PubMed]
    [Google Scholar]
  31. Pouteau-Thouvenot M., Gaudemer A., Barbier M. 1965; [On ferrorosamine, pigment of Bacillus roseus fluorescens]. Bull Soc Chim Biol (Paris) 47:2085–2094 (in French) [PubMed]
    [Google Scholar]
  32. Rezzonico F., Vogel G., Duffy B., Tonolla M. 2010; Application of whole-cell matrix-assisted laser desorption ionization-time of flight mass spectrometry for rapid identification and clustering analysis of Pantoea species. Appl Environ Microbiol 76:4497–4509 [View Article][PubMed]
    [Google Scholar]
  33. San Millan A., Santos-Lopez A., Ortega-Huedo R., Bernabe-Balas C., Kennedy S. P., Gonzalez-Zorn B. 2015; Small-plasmid-mediated antibiotic resistance is enhanced by increases in plasmid copy number and bacterial fitness. Antimicrob Agents Chemother 59:3335–3341 [View Article][PubMed]
    [Google Scholar]
  34. Schwyn B., Neilands J. B. 1987; Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56 [View Article][PubMed]
    [Google Scholar]
  35. Shiman R., Neilands J. B. 1965; Isolation, characterization, and synthesis of pyrimine, an iron (II)-binding agent from Pseudomonas GH. Biochemistry 4:2233–2236 [View Article]
    [Google Scholar]
  36. Sholberg P. L., Bedford K. E., Haag P., Randal P. 2001; Survey of Erwinia amylovora isolates from British Columbia for resistance to bactericides and virulence on apple. Can J Plant Pathol 23:60–67 [View Article]
    [Google Scholar]
  37. Simon R., Priefer U., Pühler A. 1988; A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Nat Biotechnol 1:784–785 [View Article]
    [Google Scholar]
  38. Skorupski K., Taylor R. K. 1996; Positive selection vectors for allelic exchange. Gene 169:47–52 [View Article][PubMed]
    [Google Scholar]
  39. Smits T. H. M., Duffy B. 2011; Genomics of iron acquisition in the plant pathogen Erwinia amylovora: insights in the biosynthetic pathway of the siderophore desferrioxamine E. Arch Microbiol 193:693–699 [View Article][PubMed]
    [Google Scholar]
  40. Stockwell V. O., Hockett K., Marie C., Duffy B. 2008; Pink Erwinia amylovora: colony discoloration in diagnostic isolation by co-cultured bacteria. Acta Hortic 793:539–541 [View Article]
    [Google Scholar]
  41. Vande Woestyne M., Bruyneel B., Mergeay M., Verstraete W. 1991; The Fe chelator proferrorosamine A is essential for the siderophore-mediated uptake of iron by Pseudomonas roseus fluorescens . Appl Environ Microbiol 57:949–954[PubMed]
    [Google Scholar]
  42. Vande Woestyne M., Bruyneel B., Verstraete W. 1992; Physicochemical characterization of the microbial Fe2+ chelator proferrorosamine from Pseudomonas roseus fluorescens . J Appl Bacteriol 72:44–50
    [Google Scholar]
  43. Vanneste J. L. 2000 Fire blight: The disease and its causative agent Erwinia amylovora Wallingford, UK: CABI;
  44. Zhu Y., Fu P., Lin Q., Zhang G., Zhang H., Li S., Ju J., Zhu W., Zhang C. 2012; Identification of caerulomycin A gene cluster implicates a tailoring amidohydrolase. Org Lett 14:2666–2669 [View Article][PubMed]
    [Google Scholar]
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