Home LiteratureArticle Details
PMID: 8759851 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Identification and characterization of iron-regulated Bordetella pertussis alcaligin siderophore biosynthesis genes.

Journal of bacteriology ·Vol. 178 ·No. 16 ·1996-08-00 ·Pages 4877-84

Kang HY, Brickman TJ, Beaumont FC, Armstrong SK

Abstract

Bordetella bronchiseptica mutants BRM1, BRM6, and BRM9 fail to produce the native dihydroxamate siderophore alcaligin. A 4.5-kb BamHI-Smal Bordetella pertussis genomic DNA fragment carried multiple genes required to restore alcaligin production to these siderophore-deficient mutants. Phenotypic complementation analysis using subclones of the 4.5-kb genomic region demonstrated that the closely linked BRM1 and BRM9 mutations were genetically separable from the BRM6 mutation, and both insertions exerted strong polar effects on expression of the downstream gene defined by the BRM6 mutation, suggesting a polycistronic transcriptional organization of these alcaligin biosynthesis genes. Subcloning and complementation experiments localized the putative Bordetella promoter to a 0.7-kb BamHI-SphI subregion of the cloned genomic DNA fragment. Nucleotide sequencing, phenotypic analysis of mutants, and protein expression by the 4.5-kb DNA fragment in Escherichia coli suggested the presence of three alcaligin system genes, namely, alcA, alcB, and alcC. The deduced protein products of alcA, alcB, and alcC have significant primary amino acid sequence similarities with known microbial siderophore biosynthesis enzymes. Primer extension analysis mapped the transcriptional start site of the putative alcaligin biosynthesis operon containing alcABC to a promoter region overlapping a proposed Fur repressor-binding site and demonstrated iron regulation at the transcriptional level.

MeSH Terms
Amino Acid Sequence Base Sequence Bordetella bronchiseptica/genetics,metabolism Bordetella pertussis/drug effects,genetics,metabolism Conjugation, Genetic DNA Primers DNA, Bacterial/chemistry,genetics Escherichia coli/genetics Gene Expression Regulation, Bacterial/drug effects Genes, Bacterial Hydroxamic Acids Iron/pharmacology Molecular Sequence Data Multigene Family Oligonucleotides, Antisense Operon Restriction Mapping Siderophores/biosynthesis,genetics Transcription, Genetic
Chemicals
DNA Primers DNA, Bacterial Hydroxamic Acids Oligonucleotides, Antisense Siderophores alcaligin Iron
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Kang H Y
Department of Microbiology and Immunology, East Carolina University School of Medicine, Greenville, North Carolina 27858-4354, USA.
Brickman T J
Beaumont F C
Armstrong S K
References (45)
45 references, click to expand
  1. Effect of pyridines on phenotypic properties of Bordetella pertussis.
    Infect Immun. 1982 Nov;38(2):548-53 PMID: 6292105
  2. 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):903-7 PMID: 8430103
  3. 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):1074-8 PMID: 3156376
  4. Aerobactin biosynthesis and transport genes of plasmid ColV-K30 in Escherichia coli K-12.
    J Bacteriol. 1986 Feb;165(2):570-8 PMID: 2935523
  5. Genetic diversity and relationships in populations of Bordetella spp.
    J Bacteriol. 1986 Apr;166(1):230-7 PMID: 3957867
  6. Analysis of transcription of the exotoxin A gene of Pseudomonas aeruginosa.
    J Bacteriol. 1986 Dec;168(3):1112-9 PMID: 2430945
  7. Effect of iron on accumulation of exotoxin A-specific mRNA in Pseudomonas aeruginosa.
    J Bacteriol. 1986 Dec;168(3):1451-6 PMID: 2430950
  8. Cloning of the filamentous hemagglutinin of Bordetella pertussis and its expression in Escherichia coli.
    Infect Immun. 1987 Jan;55(1):154-61 PMID: 2878885
  9. Universal chemical assay for the detection and determination of siderophores.
    Anal Biochem. 1987 Jan;160(1):47-56 PMID: 2952030
  10. Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor.
    J Bacteriol. 1987 Jun;169(6):2624-30 PMID: 3294800
  11. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  12. 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
  13. 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 PMID: 3275632
  14. Loss of transferrin receptor activity in Neisseria meningitidis correlates with inability to use transferrin as an iron source.
    Infect Immun. 1988 Dec;56(12):3132-8 PMID: 3141281
  15. Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria.
    Gene. 1988 Oct 15;70(1):191-7 PMID: 2853689
  16. Sequences required for expression of Bordetella pertussis virulence factors share homology with prokaryotic signal transduction proteins.
    Proc Natl Acad Sci U S A. 1989 Sep;86(17):6671-5 PMID: 2549542
  17. Unified approach to alignment and phylogenies.
    Methods Enzymol. 1990;183:626-45 PMID: 2314296
  18. Isolation and characterization of Bordetella bronchiseptica mutants deficient in siderophore activity.
    J Bacteriol. 1993 Feb;175(4):1144-52 PMID: 8381782
  19. Role of iron in regulation of virulence genes.
    Clin Microbiol Rev. 1993 Apr;6(2):137-49 PMID: 8472246
  20. 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):1128-40 PMID: 8106324
  21. Fur regulon in gram-negative bacteria. Identification and characterization of new iron-regulated Escherichia coli genes by a fur titration assay.
    J Mol Biol. 1994 Feb 18;236(2):531-45 PMID: 8107138
  22. Use of conditionally counterselectable suicide vectors for allelic exchange.
    Methods Enzymol. 1994;235:458-65 PMID: 8057916
  23. pBBR1MCS: a broad-host-range cloning vector.
    Biotechniques. 1994 May;16(5):800-2 PMID: 8068328
  24. The role of iron-binding proteins in the survival of pathogenic bacteria.
    Annu Rev Nutr. 1994;14:471-93 PMID: 7946530
  25. Boiling eliminates artifact banding when sequencing double-stranded templates.
    Biotechniques. 1994 Aug;17(2):288, 290 PMID: 7980929
  26. Bordetella pertussis fur gene restores iron repressibility of siderophore and protein expression to deregulated Bordetella bronchiseptica mutants.
    J Bacteriol. 1995 Jan;177(1):268-70 PMID: 7798143
  27. Identification of alcaligin as the siderophore produced by Bordetella pertussis and B. bronchiseptica.
    J Bacteriol. 1995 Feb;177(4):1116-8 PMID: 7860593
  28. Three kanamycin resistance gene cassettes with different polylinkers.
    Biotechniques. 1995 Jan;18(1):52, 54, 56 PMID: 7702853
  29. bvg Repression of alcaligin synthesis in Bordetella bronchiseptica is associated with phylogenetic lineage.
    J Bacteriol. 1995 Nov;177(21):6058-63 PMID: 7592367
  30. Siderophores: structure and function of microbial iron transport compounds.
    J Biol Chem. 1995 Nov 10;270(45):26723-6 PMID: 7592901
  31. The ornithine decarboxylase gene odc is required for alcaligin siderophore biosynthesis in Bordetella spp.: putrescine is a precursor of alcaligin.
    J Bacteriol. 1996 Jan;178(1):54-60 PMID: 8550442
  32. Identification of alcA, a Bordetella bronchiseptica gene necessary for alcaligin production.
    Gene. 1995 Dec 29;167(1-2):133-6 PMID: 8566764
  33. Purification, spectroscopic analysis and biological activity of the macrocyclic dihydroxamate siderophore alcaligin produced by Bordetella pertussis and Bordetella bronchiseptica.
    Biometals. 1996 Apr;9(2):191-203 PMID: 8744901
  34. Growth and siderophore production by Bordetella pertussis under iron-restricted conditions.
    FEMS Microbiol Lett. 1990 Jan 1;54(1-3):101-5 PMID: 2138989
  35. Siderophore-independent acquisition of transferrin-bound iron by Haemophilus influenzae type b.
    J Gen Microbiol. 1990 May;136(5):927-33 PMID: 2143216
  36. Genetic evidence that Neisseria gonorrhoeae produces specific receptors for transferrin and lactoferrin.
    J Bacteriol. 1990 Sep;172(9):5225-35 PMID: 2168377
  37. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  38. Iron-dependent regulation of diphtheria toxin and siderophore expression by the cloned Corynebacterium diphtheriae repressor gene dtxR in C. diphtheriae C7 strains.
    Infect Immun. 1991 Jun;59(6):1899-904 PMID: 1828057
  39. Siderophore production and membrane alterations by Bordetella pertussis in response to iron starvation.
    Infect Immun. 1992 Jan;60(1):117-23 PMID: 1309510
  40. A simple chemically defined medium for the production of phase I Bordetella pertussis.
    J Gen Microbiol. 1970 Oct;63(2):211-20 PMID: 4324651
  41. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  42. 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):1648-52 PMID: 377280
  43. The significance of iron in infection.
    Rev Infect Dis. 1981 Nov-Dec;3(6):1127-38 PMID: 7043704
  44. The bvg-dependent promoters show similar behaviour in different Bordetella species and share sequence homologies.
    Mol Microbiol. 1991 Oct;5(10):2493-8 PMID: 1791761
  45. Compilation and analysis of Escherichia coli promoter DNA sequences.
    Nucleic Acids Res. 1983 Apr 25;11(8):2237-55 PMID: 6344016
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1996-08-00
Pages
4877-84
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC178270
Subset
IM
Grants
NIAID NIH HHS · AI-31088 · United States
Databases
GENBANK
U32117, U34894, X76100
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: product@genelibs.com