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. 1996 Jan;178(1):54–60. doi: 10.1128/jb.178.1.54-60.1996

The ornithine decarboxylase gene odc is required for alcaligin siderophore biosynthesis in Bordetella spp.: putrescine is a precursor of alcaligin.

T J Brickman 1, S K Armstrong 1
PMCID: PMC177620  PMID: 8550442

Abstract

Chromosomal insertions defining Bordetella bronchiseptica siderophore phenotypic complementation group III mutants BRM3 and BRM5 were found to reside approximately 200 to 300 bp apart by restriction mapping of cloned genomic regions associated with the insertion markers. DNA hybridization analysis using B. bronchiseptica genomic DNA sequences flanking the cloned BRM3 insertion marker identified homologous Bordetella pertussis UT25 cosmids that complemented the siderophore biosynthesis defect of the group III B. bronchiseptica mutants. Subcloning and complementation analysis localized the complementing activity to a 2.8-kb B. pertussis genomic DNA region. Nucleotide sequencing identified an open reading frame predicted to encode a polypeptide exhibiting strong similarity at the primary amino acid level with several pyridoxal phosphate-dependent amino acid decarboxylases. Alcaligin production was fully restored to group III mutants by supplementation of iron-depleted culture media with putrescine (1,4-diaminobutane), consistent with defects in an ornithine decarboxylase activity required for alcaligin siderophore biosynthesis. Concordantly, the alcaligin biosynthesis defect of BRM3 was functionally complemented by the heterologous Escherichia coli speC gene encoding an ornithine decarboxylase activity. Enzyme assays confirmed that group III B. bronchiseptica siderophore-deficient mutants lack an ornithine decarboxylase activity required for the biosynthesis of alcaligin. Siderophore production by an analogous mutant of B. pertussis constructed by allelic exchange was undetectable. We propose the designation odc for the gene defined by these mutations that abrogate alcaligin siderophore production. Putrescine is an essential precursor of alcaligin in Bordetella spp.

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Selected References

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  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Armstrong S. K., Clements M. O. Isolation and characterization of Bordetella bronchiseptica mutants deficient in siderophore activity. J Bacteriol. 1993 Feb;175(4):1144–1152. doi: 10.1128/jb.175.4.1144-1152.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bergeron R. J., Weimar W. R. Increase in spermine content coordinated with siderophore production in Paracoccus denitrificans. J Bacteriol. 1991 Apr;173(7):2238–2243. doi: 10.1128/jb.173.7.2238-2243.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Boyle S. M., Markham G. D., Hafner E. W., Wright J. M., Tabor H., Tabor C. W. Expression of the cloned genes encoding the putrescine biosynthetic enzymes and methionine adenosyltransferase of Escherichia coli (speA, speB, speC and metK). Gene. 1984 Oct;30(1-3):129–136. doi: 10.1016/0378-1119(84)90113-6. [DOI] [PubMed] [Google Scholar]
  6. Brickman T. J., Armstrong S. K. Bordetella pertussis fur gene restores iron repressibility of siderophore and protein expression to deregulated Bordetella bronchiseptica mutants. J Bacteriol. 1995 Jan;177(1):268–270. doi: 10.1128/jb.177.1.268-270.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brown D. R., Parker C. D. Cloning of the filamentous hemagglutinin of Bordetella pertussis and its expression in Escherichia coli. Infect Immun. 1987 Jan;55(1):154–161. doi: 10.1128/iai.55.1.154-161.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bullock J. O., Armstrong S. K., Shear J. L., Lies D. P., McIntosh M. A. Formation of ion channels by colicin B in planar lipid bilayers. J Membr Biol. 1990 Mar;114(1):79–95. doi: 10.1007/BF01869387. [DOI] [PubMed] [Google Scholar]
  9. Cano-Canchola C., Sosa L., Fonzi W., Sypherd P., Ruiz-Herrera J. Developmental regulation of CUP gene expression through DNA methylation in Mucor spp. J Bacteriol. 1992 Jan;174(2):362–366. doi: 10.1128/jb.174.2.362-366.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cohen S. N., Chang A. C., Hsu L. Nonchromosomal antibiotic resistance in bacteria: genetic transformation of Escherichia coli by R-factor DNA. Proc Natl Acad Sci U S A. 1972 Aug;69(8):2110–2114. doi: 10.1073/pnas.69.8.2110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Figurski D. H., Helinski D. R. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1648–1652. doi: 10.1073/pnas.76.4.1648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Griffiths G. L., Sigel S. P., Payne S. M., Neilands J. B. Vibriobactin, a siderophore from Vibrio cholerae. J Biol Chem. 1984 Jan 10;259(1):383–385. [PubMed] [Google Scholar]
  13. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  14. Herrero M., de Lorenzo V., Neilands J. B. Nucleotide sequence of the iucD gene of the pColV-K30 aerobactin operon and topology of its product studied with phoA and lacZ gene fusions. J Bacteriol. 1988 Jan;170(1):56–64. doi: 10.1128/jb.170.1.56-64.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kameyama T., Takahashi A., Kurasawa S., Ishizuka M., Okami Y., Takeuchi T., Umezawa H. Bisucaberin, a new siderophore, sensitizing tumor cells to macrophage-mediated cytolysis. I. Taxonomy of the producing organism, isolation and biological properties. J Antibiot (Tokyo) 1987 Dec;40(12):1664–1670. doi: 10.7164/antibiotics.40.1664. [DOI] [PubMed] [Google Scholar]
  16. Kashiwagi K., Suzuki T., Suzuki F., Furuchi T., Kobayashi H., Igarashi K. Coexistence of the genes for putrescine transport protein and ornithine decarboxylase at 16 min on Escherichia coli chromosome. J Biol Chem. 1991 Nov 5;266(31):20922–20927. [PubMed] [Google Scholar]
  17. Keen N. T., Tamaki S., Kobayashi D., Trollinger D. Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene. 1988 Oct 15;70(1):191–197. doi: 10.1016/0378-1119(88)90117-5. [DOI] [PubMed] [Google Scholar]
  18. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  19. Litwin C. M., Calderwood S. B. Role of iron in regulation of virulence genes. Clin Microbiol Rev. 1993 Apr;6(2):137–149. doi: 10.1128/cmr.6.2.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mei B., Budde A. D., Leong S. A. sid1, a gene initiating siderophore biosynthesis in Ustilago maydis: molecular characterization, regulation by iron, and role in phytopathogenicity. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):903–907. doi: 10.1073/pnas.90.3.903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Meng S. Y., Bennett G. N. Nucleotide sequence of the Escherichia coli cad operon: a system for neutralization of low extracellular pH. J Bacteriol. 1992 Apr;174(8):2659–2669. doi: 10.1128/jb.174.8.2659-2669.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Moore C. H., Foster L. A., Gerbig D. G., Jr, Dyer D. W., Gibson B. W. Identification of alcaligin as the siderophore produced by Bordetella pertussis and B. bronchiseptica. J Bacteriol. 1995 Feb;177(4):1116–1118. doi: 10.1128/jb.177.4.1116-1118.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Morris D. R., Pardee A. B. Multiple pathways of putrescine biosynthesis in Escherichia coli. J Biol Chem. 1966 Jul 10;241(13):3129–3135. [PubMed] [Google Scholar]
  24. Ong S. A., Peterson T., Neilands J. B. Agrobactin, a siderophore from Agrobacterium tumefaciens. J Biol Chem. 1979 Mar 25;254(6):1860–1865. [PubMed] [Google Scholar]
  25. Schneider D. R., Parker C. D. Effect of pyridines on phenotypic properties of Bordetella pertussis. Infect Immun. 1982 Nov;38(2):548–553. doi: 10.1128/iai.38.2.548-553.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Schwyn B., Neilands J. B. Universal chemical assay for the detection and determination of siderophores. Anal Biochem. 1987 Jan;160(1):47–56. doi: 10.1016/0003-2697(87)90612-9. [DOI] [PubMed] [Google Scholar]
  27. Stainer D. W., Scholte M. J. A simple chemically defined medium for the production of phase I Bordetella pertussis. J Gen Microbiol. 1970 Oct;63(2):211–220. doi: 10.1099/00221287-63-2-211. [DOI] [PubMed] [Google Scholar]
  28. Stibitz S., Black W., Falkow S. The construction of a cloning vector designed for gene replacement in Bordetella pertussis. Gene. 1986;50(1-3):133–140. doi: 10.1016/0378-1119(86)90318-5. [DOI] [PubMed] [Google Scholar]
  29. Stim K. P., Bennett G. N. Nucleotide sequence of the adi gene, which encodes the biodegradative acid-induced arginine decarboxylase of Escherichia coli. J Bacteriol. 1993 Mar;175(5):1221–1234. doi: 10.1128/jb.175.5.1221-1234.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tabor C. W., Tabor H., Hafner E. H. Mass screening for mutants in the biosynthetic pathway for polyamines in Escherichia coli: a general method for mutants in enzymatic reactions producing CO2. Methods Enzymol. 1983;94:83–91. doi: 10.1016/s0076-6879(83)94014-4. [DOI] [PubMed] [Google Scholar]
  31. Tabor H., Tabor C. W., Hafner E. W. Convenient method for detecting 14CO2 in multiple samples: application to rapid screening for mutants. J Bacteriol. 1976 Oct;128(1):485–486. doi: 10.1128/jb.128.1.485-486.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tabor S., Richardson C. C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1074–1078. doi: 10.1073/pnas.82.4.1074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tait G. H. The identification and biosynthesis of siderochromes formed by Micrococcus denitrificans. Biochem J. 1975 Jan;146(1):191–204. doi: 10.1042/bj1460191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Takahashi A., Nakamura H., Kameyama T., Kurasawa S., Naganawa H., Okami Y., Takeuchi T., Umezawa H., Iitaka Y. Bisucaberin, a new siderophore, sensitizing tumor cells to macrophage-mediated cytolysis. II. Physico-chemical properties and structure determination. J Antibiot (Tokyo) 1987 Dec;40(12):1671–1676. doi: 10.7164/antibiotics.40.1671. [DOI] [PubMed] [Google Scholar]
  35. Tolmasky M. E., Actis L. A., Crosa J. H. A histidine decarboxylase gene encoded by the Vibrio anguillarum plasmid pJM1 is essential for virulence: histamine is a precursor in the biosynthesis of anguibactin. Mol Microbiol. 1995 Jan;15(1):87–95. doi: 10.1111/j.1365-2958.1995.tb02223.x. [DOI] [PubMed] [Google Scholar]
  36. Tolmasky M. E., Wertheimer A. M., Actis L. A., Crosa J. H. Characterization of the Vibrio anguillarum fur gene: role in regulation of expression of the FatA outer membrane protein and catechols. J Bacteriol. 1994 Jan;176(1):213–220. doi: 10.1128/jb.176.1.213-220.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Visca P., Ciervo A., Orsi N. Cloning and nucleotide sequence of the pvdA gene encoding the pyoverdin biosynthetic enzyme L-ornithine N5-oxygenase in Pseudomonas aeruginosa. J Bacteriol. 1994 Feb;176(4):1128–1140. doi: 10.1128/jb.176.4.1128-1140.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wang G., Blakesley R. W., Berg D. E., Berg C. M. pDUAL: a transposon-based cosmid cloning vector for generating nested deletions and DNA sequencing templates in vivo. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7874–7878. doi: 10.1073/pnas.90.16.7874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Weinberg E. D. Iron and infection. Microbiol Rev. 1978 Mar;42(1):45–66. doi: 10.1128/mr.42.1.45-66.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Weinberg E. D. Iron withholding: a defense against infection and neoplasia. Physiol Rev. 1984 Jan;64(1):65–102. doi: 10.1152/physrev.1984.64.1.65. [DOI] [PubMed] [Google Scholar]
  41. de Lorenzo V., Herrero M., Jakubzik U., Timmis K. N. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol. 1990 Nov;172(11):6568–6572. doi: 10.1128/jb.172.11.6568-6572.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]

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