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

Journal of Bacteriology

Volumn 179, Issue 22, 1997, Pages 7055-7062

  Wyckoff, Elizabeth E ^a   Stoebner, Janice A ^a   Reed, Kelynne E ^a,b   Payne, Shelley M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b AUSTIN COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SIDEROPHORE; VIBRIOBACTIN;

ARTICLE; BACTERIAL GROWTH; GENE CLUSTER; GENE EXPRESSION; IRON METABOLISM; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; VIBRIO CHOLERAE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; VIBRIO CHOLERAE;

EID: 0030729715     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.22.7055-7062.1997     Document Type: Article

References (64)

1. Adler, H. I., W. D. Fisher, A. Cohen, and A. A. Hardigree. 1967. Miniature Escherichia coli cells deficient in DNA. Proc. Natl. Acad. Sci. USA 57:321-326.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Andrus, C. R., M. Walter, J. H. Crosa, and S. Payne. 1983. Synthesis of siderophores by pathogenic Vibrio species. Curr. Microbiol, 9:209-214.
4. Arnow, L. E. 1937. Colorimetric determination of the components of 3,4-dihydroxyphenylalanine tyrosine mixtures. J. Biol. Chem. 118:531-537.
5. Barghouthi, S., S. M. Payne, J. E. L. Arceneaux, and B. R. Byers. 1991. Cloning, mutagenesis, and nucleotide sequence of a siderophore biosynthetic gene (amoA) from Aeromonas hydrophila. J. Bacteriol. 173:5121-5128.
6. Barghouthi, S., R. Young, M. O. J. Olson, J. E. L. Arceneaux, L. W. Clem, and B. R. Byers. 1989. Amonabactin, a novel tryptophan-or phenylalanine-containing phenolate siderophore in Aeromonas hydrophila. J. Bacteriol. 171:1811-1816.
7. Boyer, H. W., and D. Roulland-Dussoix. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472.
8. Bryce, G. F., and N. Brot. 1972. Studies on the enzymatic synthesis of the cyclic trimer of 2,3-dihydroxy-N-benzoyl-L-serine in Escherichia coli. Biochemistry 11:1708-1715.
9. Butterton, J. R., and S. B. Calderwood. 1994. Identification, cloning, and sequencing of a gene required for ferric vibriobactin utilization by Vibrio cholerae. J. Bacteriol. 176:5631-5638.
10. Butterton, J. R., J. A. Stoebner, S. M. Payne, and S. B. Calderwood. 1992. Cloning, sequencing, and transcriptional regulation of viuA, the gene encoding the ferric vibriobactin receptor of Vibrio cholerae. J. Bacteriol. 174:3729-3738.
11. Calderwood, S. B., and J. J. Mekalanos. 1987. Iron regulation of Shiga-like toxin expression in Escherichia coli is mediated by the fur locus. J. Bacteriol. 169:4759-4764.
12. 2) biosynthesis encoded by menF gene. FEMS Microbiol. Lett. 140:159-163.
13. Daskaleros, P. A., J. A. Stoebner, and S. M. Payne. 1991. Iron uptake in Plesiomonas shigelloides: cloning of the genes for the heme-iron uptake system. Infect. Immun. 59:2706-2711.
14. Earhart, C. F. 1996. Uptake and metabolism of iron and molybdenum, p. 1075-1090. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington, D.C.
15. Elkins, M. F., and C. F. Earhart. 1988. An Escherichia coli enterobactin cluster gene with sequence homology to trpE and pabB. FEMS Microbiol. Lett. 56:35-40.
16. Gay, P., D. Le Coq, M. Steinmetz, T. Berkelman, and C. I. Kado. 1985. Positive selection procedure for entrapment of insertion sequence elements in gram-negative bacteria. J. Bacteriol. 164:918-921.
17. Goldberg, M. B., V. J. DiRita, and S. B. Calderwood. 1990. Identification of an iron-regulated virulence determinant in Vibrio cholerae, using TaphoA mutagenesis. Infect. Immun. 58:55-60.
18. Griffiths, G. L., S. P. Sigel, S. M. Payne, and J. B. Neilands. 1984. Vibriobactin, a siderophore from Vibrio cholerae. J. Biol. Chem. 259:383-385.
19. 0 and Escherichia coli entD genes. J. Bacteriol. 175:6203-6211.
20. Henderson, D. P., and S. M. Payne. 1993. Cloning and characterization of the Vibrio cholerae genes encoding the utilization of iron from haemin and haemoglobin. Mol. Microbiol. 7:461-469.
21. Henderson, D. P., and S. M. Payne. 1994. Vibrio cholerae iron transport systems: role of heme and siderophore iron transport in virulence and identification of a gene associated with multiple iron transport systems. Infect. Immun. 62:5120-5125.
22. Klebba, P. E., J. M. Rutz, J. Liu, and C. K. Murphy. 1993. Mechanisms of TonB-catalyzed iron transport through the enteric bacterial cell envelop. J. Bioenerg. Biomembr. 25:603-611.
23. Lankford, C. E. 1973. Bacterial assimilation of iron. Crit. Rev. Microbiol. 2:273-331.
24. Lawlor, K. M., P. A. Daskaleros, R. E. Robinson, and S. M. Payne. 1987. Virulence of iron transport mutants of Shigella flexneri and utilization of host iron compounds. Infect. Immun. 55:594-599.
25. Litwin, C. M., T. W. Rayback, and J. Skinner. 1996. Role of catechol siderophore synthesis in Vibrio vulnificus virulence. Infect. Immun. 64:2834-2838.
26. Liu, J., K. Duncan, and C. T. Walsh. 1989. 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 dehydroge-nase. J. Bacteriol. 171:791-798.
27. Liu, J., N. Quinn, G. A. Berchtold, and C. T. Walsh. 1990. Overexpression, purification, and characterization of isochorismate synthase (EntC), the first enzyme involved in the biosynthesis of enterobactin from chorismate. Biochemistry 29:1417-1425.
28. Luke, R. K. J., and F. Gibson. 1971. Location of three genes concerned with the conversion of 2,3-dihydroxybenzoate into enterochelin in Escherichia coli K-12. J. Bacteriol. 107:557-562.
29. Marmur, J. 1961. A procedure for the isolation of deoxyribonucleic acid from microorganisms. J. Mol. Biol. 3:208-218.
30. McIntosh, M. A., C. L. Pickett, S. S. Chenault, and C. F. Earhart 1978. Suppression of iron uptake deficiency in Escherichia coli K-12 by loss of two major outer membrane proteins. Biochem. Biophys. Res. Commun. 81:1106-1112.
31. Mills, M., and S. M. Payne. 1995. Genetics and regulation of heme iron transport in Shigella dysenteriae and detection of an analogous system in Escherichia coli O157:H7. J. Bacteriol. 177:3004-3009.
32. Nahlik, M. S., T. J. Brickman, B. A. Ozenburger, and M. A. McIntosh. 1989. Nucleotide sequence and transcriptional organization of the Escherichia coli enterobactin biosynthesis cistrons entB and entA. J. Bacteriol. 171:784-790.
33. O'Brien, I. G., and F. Gibson. 1970. The structure of enterochelin and related 2,3-dihydroxy-N-benzoylserine conjugates from Escherichia coli. Biochim. Biophys. Acta 215:393-402.
34. Ozenberger, B. A., T. J. Brickman, and M. A. McIntosh. 1989. Nucleotide sequence of Escherichia coli isochorismate synthetase gene entC and evolutionary relationship of isochorismate synthetase and other chorismate-utilizing enzymes. J. Bacteriol. 171:775-783.
35. Pickett, C. L., L. Hayes, and C. F. Earhart. 1984. Molecular cloning of the Escherichia coli K-12 entACGBE genes. FEMS Microbiol. Lett. 24:77-80.
36. Pierce, J. R., C. L. Pickett, and C. F. Earhart. 1983. Two fep genes are required for ferrienterochelin uptake in Escherichia coli K-12. J. Bacteriol. 155:330-336.
37. Pollack, J. R., and J. B. Neilands. 1970. Enterobactin, an iron transport compound from Salmonella typhimurium. Biochem. Biophys. Res. Commun. 38:989-992.
38. Postle, K. 1993. TonB protein and energy transduction between membranes. J. Bioenerg. Biomembr. 25:591-601.
39. Rogers, H. J. 1973. Iron-binding catechols and virulence in Escherichia coli. Infect. Immun. 7:445-456.
40. Rowland, B. M., T. H. Grossman, M. S. Osburne, and H. W. Tabor. 1996. Sequence and genetic organization of a Bacillus subtilis operon encoding 2,3-dihydroxybenzoate biosynthetic enzymes. Gene 178:119-123.
41. Rusnak, F., W. S. Faraci, and C. T. Walsh. 1989. Subcloning, expression, and purification of the enterobactin biosynthetic enzyme 2,3-dihydroxybenzoate-AMP ligase: demonstration of enzyme-bound (2,3-dihydroxybenzoyl)adenylate product. Biochemistry 28:6827-6835.
42. Rusnak, F., J. Liu, N. Quinn, G. A. Berchtold, and C. T. Walsh. 1990. Subcloning of the enterobactin biosynthetic gene entB: expression, purification, characterization, and substrate specificity of isochorismatase. Biochemistry 29:1425-1435.
43. Sakaitani, M., F. Rusnak, N. R. Quinn, C. Tu, T. B. Frigo, G. A. Berchtold, and C. T. Walsh. 1990. Mechanistic studies on trans-2,3-dihydroxybenzoate dehydrogenase (EntA) in the biosynthesis of the iron chelator enterobactin. Biochemistry 29:6789-6798.
44. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
45. Schmitt, M. P., and S. M. Payne. 1991. Genetic analysis of the enterobactin gene cluster in Shigella flexneri. J. Bacteriol. 173:816-825.
46. Schmitt, M. P., and S. M. Payne. 1988. Genetics and regulation of enterobactin genes in Shigella flexneri. J. Bacteriol. 170:5579-5587.
47. Schwyn, B., and J. B. Neilands. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:47-56.
48. Serino, L., C. Reimmann, H. Baur, M. Beyeler, P. Visca, and D. Haas. 1995. Structural genes for salicylate biosynthesis from chorismate in Pseudomonas aeruginosa. Mol. Gen. Genet. 249:217-228.
49. Sigel, S. P., and S. M. Payne. 1982. Effect of iron limitation on growth, siderophore production, and expression of outer membrane proteins of Vibrio cholerae. J. Bacteriol. 150:148-155.
50. Sigel, S. P., J. A. Stoebner, and S. M. Payne. 1985. Iron-vibriobactin transport system is not required for virulence of Vibrio cholerae. Infect, Immun. 47:360-362.
51. Simpson, L. M., M. A. Dry, and J. D. Oliver. 1987. Experimental Vibrio cholerae wound infections. FEMS Microbiol. Lett. 40:89-93.
52. Staab, J. F., and C. F. Earhart. 1990. EntG activity of Escherichia coli enterobactin synthetase. J. Bacteriol. 172:6403-6410.
53. Staab, J. F., M. F. Elkins, and C. F. Earhart. 1989. Nucleotide sequence of the Escherichia coli entE gene. FEMS Microbiol. Lett. 59:15-20.
54. Stoebner, J. A., J. R. Butterton, S. B. Calderwood, and S. M. Payne. 1992. Identification of the vibriobactin receptor of Vibrio cholerae. J. Bacteriol. 174:3270-3274.
55. Stoebner, J. A., and S. M. Payne. 1988. Iron-regulated hemolysin production and utilization of heme and hemoglobin by Vibrio cholerae. Infect. Immun. 56:2891-2895.
56. Tashima, K. T., P. A. Carroll, M. B. Rogers, and S. B. Calderwood. 1996. Relative importance of three iron-regulated outer membrane proteins for in vivo growth of Vibrio cholerae. Infect. Immun. 64:1756-1761.
57. Walsh, C. T., J. Liu, F. Rusnak, and M. Sakaitani. 1990. Molecular studies on enzymes in chorismate metabolism and enterobactin biosynthetic pathway. Chem. Rev. 90:1105-1129.
58. Wang, R. F., and S. R. Kushner. 1991. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100:195-199.
59. Wilkins, T. D., and C. E. Lankford. 1970. Production by Salmonella typhimurium of 2,3-dihydroxybenzoylserine and its stimulation of growth in human serum. J. Infect. Dis. 121:129-136.
60. Woodrow, G. C., I. G. Young, and F. Gibson. 1975. 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. 124:1-6.
61. Wyckoff, E. E., and S. M. Payne. Unpublished data.
62. Yamamoto, S., S. Shinoda, M. Kawaguchi, K. Wakamatsu, and M. Makita. 1983. Polyamine distribution in Vibrionaceae: norspermidine as a general constituent of Vibrio species. Can. J. Microbiol. 29:724-728.
63. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
64. Young, I. G., L. Langman, R. K. J. Luke, and F. Gibson. 1971. Biosynthesis of the iron-transport compound enterochelin: mutants of Escherichia coli unable to synthesize 2,3-dihydroxybenzoate. J. Bacteriol. 106:51-57.