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Volume 152, Issue 12

A gene cluster involved in the biosynthesis of vanchrobactin, a chromosome-encoded siderophore produced by Free

Abstract

serotype O2 strains produce a catechol siderophore named vanchrobactin, which has been identified as -[′-(2,3-dihydroxybenzoyl)-arginyl]-serine. This work describes a chromosomal region that harbours the genetic determinants necessary for the biosynthesis of vanchrobactin. The authors have identified the genes involved in 2,3-dihydroxybenzoic acid (DHBA) biosynthesis (, and ) and activation (), and a gene () encoding a non-ribosomal peptide synthetase, which is putatively involved in the assembly of the siderophore components. Also described are the identification and characterization of genes encoding a putative vanchrobactin exporter () and a siderophore esterase (). In-frame deletion mutants in , , , , and were impaired for growth under conditions of iron limitation, and the analysis of culture supernatants by chrome azurol-S and cross-feeding assays showed almost no production of siderophores in any of the mutants. In addition, deletion mutations of , and abolished production of DHBA, as assessed by chemical and biological analyses. Complementation of each mutant with the corresponding gene provided confirmed the involvement of this gene cluster in the biosynthesis of DHBA and vanchrobactin in strain RV22. Based on chemical and genetic data, and on published models for other catechol siderophores, a model for vanchrobactin biosynthesis is proposed.

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Keyword(s): A-domain, adenylation domain , ArCP, aryl carrier protein , CAS, chrome azurol-S , DBS, 2,3-dihydroxybenzoyl-serine , DHBA, 2,3-dihydroxybenzoic acid , EDDA, ethylenediamine-di-(o-hydroxyphenylacetic acid) , MFS, major facilitator superfamily , NRPS, non-ribosomal peptide synthetase , PCP, peptidyl carrier protein and TE, thioesterase
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2006-12-01
2024-04-20
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References

  1. Alice A. F, Lopez C. S, Crosa J. H. 2005; Plasmid- and chromosome-encoded redundant and specific functions are involved in biosynthesis of the siderophore anguibactin in Vibrio anguillarum 775: a case of chance and necessity?. J Bacteriol 187:2209–2214 [CrossRef]
     [Google Scholar]
  2. Apweiler R, Bairoch A, Wu C. H. 12 other authors 2004; UniProt: the Universal Protein knowledgebase. Nucleic Acids Res 32:D115–119 [CrossRef]
     [Google Scholar]
  3. Arnow L. E. 1937; Colorimetric determination of the components of 3,4 dihydroxyphenyl-alanine-tyrosine mixtures. J Biol Chem 118:531–537
     [Google Scholar]
  4. Bateman A, Coin L, Durbin R. 10 other authors 2004; The Pfam protein families database. Nucleic Acids Res 32:D138–141 [CrossRef]
     [Google Scholar]
  5. Boeckmann B, Bairoch A, Apweiler R. 9 other authors 2003; The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res 31:365–370 [CrossRef]
     [Google Scholar]
  6. Brickman T. J, McIntosh M. A. 1992; Overexpression and purification of ferric enterobactin esterase from Escherichia coli . Demonstration of enzymatic hydrolysis of enterobactin and its iron complex. J Biol Chem 267:12350–12355
     [Google Scholar]
  7. Buss K, Muller R, Dahm C, Gaitatzis N, Skrzypczak-Pietraszek E, Lohmann S, Gassen M, Leistner E. 2001; Clustering of isochorismate synthase genes menF and entC and channeling of isochorismate in Escherichia coli . Biochim Biophys Acta 1522:151–157 [CrossRef]
     [Google Scholar]
  8. Challis G. L, Ravel J, Townsend C. A. 2000; Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem Biol 7:211–224 [CrossRef]
     [Google Scholar]
  9. Chen Q, Actis L. A, Tolmasky M. E, Crosa J. H. 1994; Chromosome-mediated 2,3-dihydroxybenzoic acid is a precursor in the biosynthesis of the plasmid-mediated siderophore anguibactin in Vibrio anguillarum . J Bacteriol 176:4226–4234
     [Google Scholar]
  10. Conchas R. F, Lemos M. L, Barja J. L, Toranzo A. E. 1991; Distribution of plasmid- and chromosome-mediated iron uptake systems in Vibrio anguillarum strains of different origins. Appl Environ Microbiol 57:2956–2962
     [Google Scholar]
  11. 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]
  12. Di Vincenzo L, Grgurina I, Pascarella S. 2005; In silico analysis of the adenylation domains of the freestanding enzymes belonging to the eucaryotic nonribosomal peptide synthetase-like family. FEBS J 272:929–941 [CrossRef]
     [Google Scholar]
  13. Dorsey C. W, Tolmasky M. E, Crosa J. H, Actis L. A. 2003; Genetic organization of an Acinetobacter baumannii chromosomal region harbouring genes related to siderophore biosynthesis and transport. Microbiology 149:1227–1238 [CrossRef]
     [Google Scholar]
  14. Earhart C. F. others 1996; Uptake and metabolism of iron and molybdenum. In Escherichia coli and Salmonella: Cellular and Molecular Biology , 2nd edn. pp.  1075–1090 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  15. Ehmann D. E, Shaw-Reid C. A, Losey H. C, Walsh C. T. 2000; The EntF and EntE adenylation domains of Escherichia coli enterobactin synthetase: sequestration and selectivity in acyl-AMP transfers to thiolation domain cosubstrates. Proc Natl Acad Sci U S A 97:2509–2514 [CrossRef]
     [Google Scholar]
  16. Felsenstein J. 1996; Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. Methods Enzymol 266:418–427
     [Google Scholar]
  17. Furrer J. L, Sanders D. N, Hook-Barnard I. G, McIntosh M. A. 2002; Export of the siderophore enterobactin in Escherichia coli : involvement of a 43 kDa membrane exporter. Mol Microbiol 44:1225–1234 [CrossRef]
     [Google Scholar]
  18. Hall T. A. 1999; bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
     [Google Scholar]
  19. Hantke K. 1990; Dihydroxybenzoylserine – a siderophore for E. coli . FEMS Microbiol Lett 55:5–8
     [Google Scholar]
  20. Herrero M, Timmis K. N, de Lorenzo V. 1990; Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in Gram-negative bacteria. J Bacteriol 172:6557–6567
     [Google Scholar]
  21. Holmstrom K, Gram L. 2003; Elucidation of the Vibrio anguillarum genetic response to the potential fish probiont Pseudomonas fluorescens AH2, using RNA-arbitrarily primed PCR. J Bacteriol 185:831–842 [CrossRef]
     [Google Scholar]
  22. Kloosterman H, Hessels G. I, Vrijbloed J. W, Euverink G. J, Dijkhuizen L. 2003; (De)regulation of key enzyme steps in the shikimate pathway and phenylalanine-specific pathway of the actinomycete Amycolatopsis methanolica . Microbiology 149:3321–3330 [CrossRef]
     [Google Scholar]
  23. Lautru S, Challis G. L. 2004; Substrate recognition by nonribosomal peptide synthetase multi-enzymes. Microbiology 150:1629–1636 [CrossRef]
     [Google Scholar]
  24. Lemos M. L, Salinas P, Toranzo A. E, Barja J. L, Crosa J. H. 1988; Chromosome-mediated iron uptake system in pathogenic strains of Vibrio anguillarum . J Bacteriol 170:1920–1925
     [Google Scholar]
  25. Marahiel M. A, Stachelhaus T, Mootz H. D. 1997; Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem Rev 97:2651–2674 [CrossRef]
     [Google Scholar]
  26. Mouriño S, Osorio C. R, Lemos M. L. 2004; Characterization of heme uptake cluster genes in the fish pathogen Vibrio anguillarum . J Bacteriol 186:6159–6167 [CrossRef]
     [Google Scholar]
  27. Pao S. S, Paulsen I. T, Saier M. H Jr. 1998; Major facilitator superfamily. Microbiol Mol Biol Rev 62:1–34
     [Google Scholar]
  28. Parales R. E, Harwood C. S. 1993; Construction and use of a new broad-host-range lacZ transcriptional fusion vector, pHRP309, for Gram− -bacteria. Gene 133:23–30 [CrossRef]
     [Google Scholar]
  29. Paulsen I. T, Brown M. H, Skurray R. A. 1996; Proton-dependent multidrug efflux systems. Microbiol Rev 60:575–608
     [Google Scholar]
  30. Pedersen K, Grisez L, Tiainen T, Ollevier F, Larsen J. L, van Houdt R. 1999; Extended serotyping scheme for Vibrio anguillarum with the definition and characterization of seven provisional O-serogroups. Curr Microbiol 38:183–189 [CrossRef]
     [Google Scholar]
  31. Pollack J. R, Ames B. N, Neilands J. B. 1970; Iron transport in Salmonella typhimurium : mutants blocked in the biosynthesis of enterobactin. J Bacteriol 104:635–639
     [Google Scholar]
  32. Rabsch W, Methner U, Voigt W, Tschape H, Reissbrodt R, Williams P. H. 2003; Role of receptor proteins for enterobactin and 2,3-dihydroxybenzoylserine in virulence of Salmonella enterica . Infect Immun 71:6953–6961 [CrossRef]
     [Google Scholar]
  33. Rausch C, Weber T, Kohlbacher O, Wohlleben W, Huson D. H. 2005; Specificity prediction of adenylation domains in nonribosomal peptide synthetases (NRPS) using transductive support vector machines (TSVMs). Nucleic Acids Res 33:5799–5808 [CrossRef]
     [Google Scholar]
  34. Rauscher L, Expert D, Matzanke B. F, Trautwein A. X. 2002; Chrysobactin-dependent iron acquisition in Erwinia chrysanthemi . Functional study of a homolog of the Escherichia coli ferric enterobactin esterase. J Biol Chem 277:2385–2395 [CrossRef]
     [Google Scholar]
  35. Reichert J, Sakaitani M, Walsh C. T. 1992; Characterization of EntF as a serine-activating enzyme. Protein Sci 1:549–556
     [Google Scholar]
  36. Rusnak F, Sakaitani M, Drueckhammer D, Reichert J, Walsh C. T. 1991; Biosynthesis of the Escherichia coli siderophore enterobactin: sequence of the entF gene, expression and purification of EntF, and analysis of covalent phosphopantetheine. Biochemistry 30:2916–2927 [CrossRef]
     [Google Scholar]
  37. Sambrook J, Russell D. W. 2001 Molecular Cloning: a Laboratory Manual , 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  38. Schwyn B, Neilands J. B. 1987; Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56 [CrossRef]
     [Google Scholar]
  39. Soengas R. G, Anta C, Espada A, Paz V, Ares I. R, Balado M, Lemos M. L, Rodríguez J, Jiménez C. 2006; Structural characterization of vanchrobactin, a new catechol siderophore produced by the fish pathogen Vibrio anguillarum serotype O2. Tetrahedron Lett 47:7113–7116 [CrossRef]
     [Google Scholar]
  40. Stachelhaus T, Mootz H. D, Marahiel M. A. 1999; The specificity-conferring code of adenylation domains in nonribosomal peptide synthetases. Chem Biol 6:493–505 [CrossRef]
     [Google Scholar]
  41. Stork M, Di Lorenzo M, Welch T. J, Crosa L. M, Crosa J. H. 2002; Plasmid-mediated iron uptake and virulence in Vibrio anguillarum . Plasmid 48:222–228 [CrossRef]
     [Google Scholar]
  42. Thompson J. D, Higgins D. G, Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [CrossRef]
     [Google Scholar]
  43. Toranzo A. E, Barja J. L. 1990; A review of the taxonomy and seroepizootiology of Vibrio anguillarum , with special reference to aquaculture in the northwest of Spain. Dis Aquat Org 9:73–82 [CrossRef]
     [Google Scholar]
  44. Toranzo A. E, Santos Y, Barja J. L. 1997; Immunization with bacterial antigens: Vibrio infections. Dev Biol Stand 90:93–105
     [Google Scholar]
  45. Tusnady G. E, Simon I. 2001; The hmmtop transmembrane topology prediction server. Bioinformatics 17:849–850 [CrossRef]
     [Google Scholar]
  46. Walsh C. T, Liu J, Rusnak F, Sakaitani M. 1990; Molecular studies on enzymes in chorismate metabolism and enterobactin biosynthetic pathway. Chem Rev 90:1105–1129 [CrossRef]
     [Google Scholar]
  47. Wandersman C, Delepelaire P. 2004; Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58:611–647 [CrossRef]
     [Google Scholar]
  48. Wang R. F, Kushner S. R. 1991; Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli . Gene 100:195–199 [CrossRef]
     [Google Scholar]
  49. Wolf M. K, Crosa J. H. 1986; Evidence for the role of a siderophore in promoting Vibrio anguillarum infections. J Gen Microbiol 132:2949–2952
     [Google Scholar]
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A gene cluster involved in the biosynthesis of vanchrobactin, a chromosome-encoded siderophore produced by Vibrio anguillarum
Microbiology 152, 3517 (2006); https://doi.org/10.1099/mic.0.29298-0
/content/journal/micro/10.1099/mic.0.29298-0
/content/journal/micro/10.1099/mic.0.29298-0
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