Home LiteratureArticle Details
PMID: 9371453 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Cloning of a Vibrio cholerae vibriobactin gene cluster: identification of genes required for early steps in siderophore biosynthesis.

Journal of bacteriology ·Vol. 179 ·No. 22 ·1997-11-00 ·Pages 7055-62

Wyckoff EE, Stoebner JA, Reed KE, Payne SM

Abstract

Vibrio cholerae secretes the catechol siderophore vibriobactin in response to iron limitation. Vibriobactin is structurally similar to enterobactin, the siderophore produced by Escherichia coli, and both organisms produce 2,3-dihydroxybenzoic acid (DHBA) as an intermediate in siderophore biosynthesis. To isolate and characterize V. cholerae genes involved in vibriobactin biosynthesis, we constructed a genomic cosmid bank of V. cholerae DNA and isolated clones that complemented mutations in E. coli enterobactin biosynthesis genes. V. cholerae homologs of entA, entB, entC, entD, and entE were identified on overlapping cosmid clones. Our data indicate that the vibriobactin genes are clustered, like the E. coli enterobactin genes, but the organization of the genes within these clusters is different. In this paper, we present the organization and sequences of genes involved in the synthesis and activation of DHBA. In addition, a V. cholerae strain with a chromosomal mutation in vibA was constructed by marker exchange. This strain was unable to produce vibriobactin or DHBA, confirming that in V. cholerae VibA catalyzes an early step in vibriobactin biosynthesis.

MeSH Terms
Catechols Chromosome Mapping Cloning, Molecular Cosmids DNA Transposable Elements DNA, Bacterial/genetics Enterobactin/metabolism Escherichia coli/genetics Gene Expression Regulation, Bacterial Gene Library Genetic Complementation Test Hydroxybenzoates/metabolism Multigene Family Mutagenesis, Insertional Oxazoles Recombination, Genetic Sequence Homology, Amino Acid Siderophores/biosynthesis,metabolism Vibrio cholerae/genetics,metabolism
Chemicals
Catechols DNA Transposable Elements DNA, Bacterial Hydroxybenzoates Oxazoles Siderophores Enterobactin 2,3-dihydroxybenzoic acid vibriobactin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Wyckoff E E
Department of Microbiology, University of Texas, Austin 78712-1095, USA.
Stoebner J A
Reed K E
Payne S M
References (52)
52 references, click to expand
  1. Nucleotide sequence of Escherichia coli isochorismate synthetase gene entC and evolutionary relationship of isochorismate synthetase and other chorismate-utilizing enzymes.
    J Bacteriol. 1989 Feb;171(2):775-83 PMID: 2536681
  2. Genetic analysis of the enterobactin gene cluster in Shigella flexneri.
    J Bacteriol. 1991 Jan;173(2):816-25 PMID: 1846151
  3. Relative importance of three iron-regulated outer membrane proteins for in vivo growth of Vibrio cholerae.
    Infect Immun. 1996 May;64(5):1756-61 PMID: 8613388
  4. Genetics and regulation of enterobactin genes in Shigella flexneri.
    J Bacteriol. 1988 Dec;170(12):5579-87 PMID: 2973458
  5. Universal chemical assay for the detection and determination of siderophores.
    Anal Biochem. 1987 Jan;160(1):47-56 PMID: 2952030
  6. The structure of enterochelin and related 2,3-dihydroxy-N-benzoylserine conjugates from Escherichia coli.
    Biochim Biophys Acta. 1970 Aug 14;215(2):393-402 PMID: 4926450
  7. Identification of an iron-regulated virulence determinant in Vibrio cholerae, using TnphoA mutagenesis.
    Infect Immun. 1990 Jan;58(1):55-60 PMID: 2152889
  8. Cloning, sequencing, and transcriptional regulation of viuA, the gene encoding the ferric vibriobactin receptor of Vibrio cholerae.
    J Bacteriol. 1992 Jun;174(11):3729-38 PMID: 1317381
  9. Production by Salmonella typhimurium of 2,3-dihydroxybenzoylserine, and its stimulation of growth in human serum.
    J Infect Dis. 1970 Feb;121(2):129-36 PMID: 4905647
  10. Effect of iron limitation on growth, siderophore production, and expression of outer membrane proteins of Vibrio cholerae.
    J Bacteriol. 1982 Apr;150(1):148-55 PMID: 6460753
  11. A complementation analysis of the restriction and modification of DNA in Escherichia coli.
    J Mol Biol. 1969 May 14;41(3):459-72 PMID: 4896022
  12. Cloning, mutagenesis, and nucleotide sequence of a siderophore biosynthetic gene (amoA) from Aeromonas hydrophila.
    J Bacteriol. 1991 Aug;173(16):5121-8 PMID: 1830579
  13. Subcloning, expression, and purification of the enterobactin biosynthetic enzyme 2,3-dihydroxybenzoate-AMP ligase: demonstration of enzyme-bound (2,3-dihydroxybenzoyl)adenylate product.
    Biochemistry. 1989 Aug 22;28(17):6827-35 PMID: 2531000
  14. Role of catechol siderophore synthesis in Vibrio vulnificus virulence.
    Infect Immun. 1996 Jul;64(7):2834-8 PMID: 8698519
  15. EntG activity of Escherichia coli enterobactin synthetase.
    J Bacteriol. 1990 Nov;172(11):6403-10 PMID: 2172214
  16. Identification of the vibriobactin receptor of Vibrio cholerae.
    J Bacteriol. 1992 May;174(10):3270-4 PMID: 1315733
  17. Structural genes for salicylate biosynthesis from chorismate in Pseudomonas aeruginosa.
    Mol Gen Genet. 1995 Nov 15;249(2):217-28 PMID: 7500944
  18. Subcloning of the enterobactin biosynthetic gene entB: expression, purification, characterization, and substrate specificity of isochorismatase.
    Biochemistry. 1990 Feb 13;29(6):1425-35 PMID: 2139796
  19. Positive selection procedure for entrapment of insertion sequence elements in gram-negative bacteria.
    J Bacteriol. 1985 Nov;164(2):918-21 PMID: 2997137
  20. Amonabactin, a novel tryptophan- or phenylalanine-containing phenolate siderophore in Aeromonas hydrophila.
    J Bacteriol. 1989 Apr;171(4):1811-6 PMID: 2522922
  21. Iron-Binding Catechols and Virulence in Escherichia coli.
    Infect Immun. 1973 Mar;7(3):445-56 PMID: 16558077
  22. Iron uptake in Plesiomonas shigelloides: cloning of the genes for the heme-iron uptake system.
    Infect Immun. 1991 Aug;59(8):2706-11 PMID: 1830293
  23. Nucleotide sequence and transcriptional organization of the Escherichia coli enterobactin biosynthesis cistrons entB and entA.
    J Bacteriol. 1989 Feb;171(2):784-90 PMID: 2521621
  24. Genetics and regulation of heme iron transport in Shigella dysenteriae and detection of an analogous system in Escherichia coli O157:H7.
    J Bacteriol. 1995 Jun;177(11):3004-9 PMID: 7768795
  25. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli.
    Gene. 1991 Apr;100:195-9 PMID: 2055470
  26. MINIATURE escherichia coli CELLS DEFICIENT IN DNA.
    Proc Natl Acad Sci U S A. 1967 Feb;57(2):321-6 PMID: 16591472
  27. Mu-induced polarity in the Escherichia coli K-12 ent gene cluster: evidence for a gene (entG) involved in the biosynthesis of enterochelin.
    J Bacteriol. 1975 Oct;124(1):1-6 PMID: 126224
  28. Sequence and genetic organization of a Bacillus subtilis operon encoding 2,3-dihydroxybenzoate biosynthetic enzymes.
    Gene. 1996 Oct 31;178(1-2):119-23 PMID: 8921902
  29. Vibrio cholerae iron transport systems: roles of heme and siderophore iron transport in virulence and identification of a gene associated with multiple iron transport systems.
    Infect Immun. 1994 Nov;62(11):5120-5 PMID: 7927795
  30. Location of three genes concerned with the conversion of 2,3-dihydroxybenzoate into enterochelin in Escherichia coli K-12.
    J Bacteriol. 1971 Aug;107(2):557-62 PMID: 4939766
  31. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  32. Identification, cloning, and sequencing of a gene required for ferric vibriobactin utilization by Vibrio cholerae.
    J Bacteriol. 1994 Sep;176(18):5631-8 PMID: 8083157
  33. Nucleotide sequence of the Escherichia coli entE gene.
    FEMS Microbiol Lett. 1989 May;50(1-2):15-9 PMID: 2525505
  34. TonB protein and energy transduction between membranes.
    J Bioenerg Biomembr. 1993 Dec;25(6):591-601 PMID: 8144488
  35. A new isochorismate synthase specifically involved in menaquinone (vitamin K2) biosynthesis encoded by the menF gene.
    FEMS Microbiol Lett. 1996 Jul 1;140(2-3):159-63 PMID: 8764478
  36. Mechanisms of TonB-catalyzed iron transport through the enteric bacterial cell envelope.
    J Bioenerg Biomembr. 1993 Dec;25(6):603-11 PMID: 8144489
  37. Mechanistic studies on trans-2,3-dihydro-2,3-dihydroxybenzoate dehydrogenase (Ent A) in the biosynthesis of the iron chelator enterobactin.
    Biochemistry. 1990 Jul 24;29(29):6789-98 PMID: 2144454
  38. Vibriobactin, a siderophore from Vibrio cholerae.
    J Biol Chem. 1984 Jan 10;259(1):383-5 PMID: 6706943
  39. Overexpression, purification, and characterization of isochorismate synthase (EntC), the first enzyme involved in the biosynthesis of enterobactin from chorismate.
    Biochemistry. 1990 Feb 13;29(6):1417-25 PMID: 2139795
  40. Studies on the enzymatic synthesis of the cyclic trimer of 2,3-dihydroxy-N-benzoyl-L-serine in Escherichia coli.
    Biochemistry. 1972 Apr 25;11(9):1708-15 PMID: 4337557
  41. Biosynthesis of the iron-transport compound enterochelin: mutants of Escherichia coli unable to synthesize 2,3-dihydroxybenzoate.
    J Bacteriol. 1971 Apr;106(1):51-7 PMID: 4928016
  42. Isolation and characterization of Bacillus subtilis genes involved in siderophore biosynthesis: relationship between B. subtilis sfpo and Escherichia coli entD genes.
    J Bacteriol. 1993 Oct;175(19):6203-11 PMID: 8407792
  43. Virulence of iron transport mutants of Shigella flexneri and utilization of host iron compounds.
    Infect Immun. 1987 Mar;55(3):594-9 PMID: 3028962
  44. Enterobactin, an iron transport compound from Salmonella typhimurium.
    Biochem Biophys Res Commun. 1970 Mar 12;38(5):989-92 PMID: 4908541
  45. Cloning and characterization of the Vibrio cholerae genes encoding the utilization of iron from haemin and haemoglobin.
    Mol Microbiol. 1993 Feb;7(3):461-9 PMID: 8384684
  46. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  47. Nucleotide sequence of a cluster of Escherichia coli enterobactin biosynthesis genes: identification of entA and purification of its product 2,3-dihydro-2,3-dihydroxybenzoate dehydrogenase.
    J Bacteriol. 1989 Feb;171(2):791-8 PMID: 2521622
  48. Iron-vibriobactin transport system is not required for virulence of Vibrio cholerae.
    Infect Immun. 1985 Feb;47(2):360-2 PMID: 3967921
  49. Iron regulation of Shiga-like toxin expression in Escherichia coli is mediated by the fur locus.
    J Bacteriol. 1987 Oct;169(10):4759-64 PMID: 3308853
  50. Two fep genes are required for ferrienterochelin uptake in Escherichia coli K-12.
    J Bacteriol. 1983 Jul;155(1):330-6 PMID: 6223021
  51. Suppression of iron uptake deficiency in Escherichia coli K-12 by loss of two major outer membrane proteins.
    Biochem Biophys Res Commun. 1978 Apr 28;81(4):1106-12 PMID: 149543
  52. Iron-regulated hemolysin production and utilization of heme and hemoglobin by Vibrio cholerae.
    Infect Immun. 1988 Nov;56(11):2891-5 PMID: 2971620
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1997-11-00
Pages
7055-62
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC179647
Subset
IM
Grants
NIAID NIH HHS · AI16935 · United States
Databases
GENBANK
U52150
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]