Abstract
The XhoI fragment containing much of the iron uptake region of plasmid pJM1 was isolated from Vibrio anguillarum 775 and cloned into plasmid pBR322. Plasmid-encoded polypeptides were examined in maxicells of Escherichia coli, and transposon mutagenesis was used to map insertion mutations in the structural DNA encoding the OM2 polypeptide. Tn1000 insertions that mapped within OM2 and blocked maxicell expression of OM2 resulted in the loss of ferric iron-anguibactin receptor function when plasmids containing OM2:: Tn1000 insertions were introduced into V. anguillarum cells. Two iron-regulated polypeptides were identified in maxicell polypeptide profiles of E. coli SS201. A 20,000-dalton polypeptide was expressed in maxicells of SS201 grown under conditions of iron limitation but was barely detectable in profiles of SS201 cells that were grown under high-iron conditions. DNA encoding the 20,000-dalton polypeptide mapped downstream of and adjacent to the gene encoding OM2. DNA sequences required for production of a 46,000-dalton polypeptide mapped 4.5 kilobases downstream of the OM2 structural gene. The 46,000-dalton polypeptide was synthesized at high levels in E. coli SS201 maxicells grown under high-iron conditions, but synthesis of the protein was severely repressed under conditions of iron limitation. Iron-regulated expression of both proteins in maxicells of SS201 was relieved upon deletion of a 4.9-kilobase SalI-XhoI fragment of pJM1 DNA, which indicated that pJM1 DNA sequences present in the deleted fragment are required for regulated expression of both proteins in E. coli. Maxicells of SS201 harboring these deletion derivatives synthesized the 20,000-dalton polypeptide at very low constitutive levels and the 46,000-dalton polypeptide at high constitutive levels, regardless of the iron concentration of the growth medium. The observed regulation of the 20,000-dalton protein suggested that it might play a role either in siderophore biosynthesis or in the functional expression of OM2. The opposite regulatory pattern observed for the 46,000-dalton polypeptide suggested that it does not play a structural role in siderophore or OM2 biosynthesis, but the observed regulatory pattern might be expected if the 46,000-dalton protein played a negative regulatory role in siderophore biosynthesis.
MeSH Terms
Bacterial Proteins/genetics
Biological Assay
Cloning, Molecular
DNA Mutational Analysis
Escherichia coli/genetics
Gene Expression Regulation
Genes
Genes, Bacterial
Iron/metabolism
Molecular Weight
Plasmids
Recombinant Proteins/metabolism
Restriction Mapping
Vibrio/genetics,pathogenicity
Chemicals
Bacterial Proteins
Recombinant Proteins
Iron
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Singer J T
Department of Microbiology, University of Maine, Orono 04469.
Earley S
References (29)
29 references, click to expand
-
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
-
Increased production of the siderophore anguibactin mediated by pJM1-like plasmids in Vibrio anguillarum.
Infect Immun. 1988 Jun;56(6):1608-14
PMID: 3372022
-
Isolation and characterization of a generalized transducing bacteriophage for Acinetobacter.
J Virol. 1974 Jan;13(1):46-52
PMID: 4129844
-
High resolution two-dimensional electrophoresis of proteins.
J Biol Chem. 1975 May 25;250(10):4007-21
PMID: 236308
-
An octamer of histones in chromatin and free in solution.
Proc Natl Acad Sci U S A. 1975 Jul;72(7):2626-30
PMID: 241077
-
Deoxyribonucleic acid relationships among marine vibrios pathogenic to fish.
Can J Microbiol. 1977 Aug;23(8):954-8
PMID: 890607
-
Evidence for plasmid contribution to the virulence of fish pathogen Vibrio anguillarum.
Infect Immun. 1977 Nov;18(2):509-13
PMID: 924679
-
The gamma delta sequence of F is an insertion sequence.
J Mol Biol. 1978 Dec 15;126(3):347-65
PMID: 745233
-
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
-
A plasmid associated with virulence in the marine fish pathogen Vibrio anguillarum specifies an iron-sequestering system.
Nature. 1980 Apr 10;284(5756):566-8
PMID: 7366725
-
Curing of a plasmid is correlated with an attenuation of virulence in the marine fish pathogen Vibrio anguillarum.
Infect Immun. 1980 Mar;27(3):897-902
PMID: 6247282
-
Outer membrane proteins induced under conditions of iron limitation in the marine fish pathogen Vibrio anguillarum 775.
Infect Immun. 1981 Jan;31(1):223-7
PMID: 7194320
-
Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti.
Proc Natl Acad Sci U S A. 1980 Dec;77(12):7347-51
PMID: 7012838
-
Identification and preliminary characterization of Treponema pallidum protein antigens expressed in Escherichia coli.
Infect Immun. 1983 Aug;41(2):709-21
PMID: 6347894
-
Uses of the transposon gamma delta in the analysis of cloned genes.
Methods Enzymol. 1983;101:362-9
PMID: 6310336
-
Iron uptake system medicated by Vibrio anguillarum plasmid pJM1.
J Bacteriol. 1983 Nov;156(2):880-7
PMID: 6313622
-
Molecular cloning and expression of genetic determinants for the iron uptake system mediated by the Vibrio anguillarum plasmid pJM1.
J Bacteriol. 1984 Dec;160(3):860-6
PMID: 6094511
-
Iron-regulated outer membrane protein OM2 of Vibrio anguillarum is encoded by virulence plasmid pJM1.
J Bacteriol. 1985 Feb;161(2):736-42
PMID: 3968037
-
Studies on deo operon regulation in Escherichia coli: cloning and expression of the deoR structural gene.
Gene. 1984 Nov;31(1-3):205-11
PMID: 6098525
-
Plasmid-mediated iron sequestering systems in pathogenic strains of Vibrio anguillarum and Escherichia coli.
Basic Life Sci. 1985;30:759-74
PMID: 2990437
-
Identification of the Escherichia coli deoR and cytR gene products.
J Bacteriol. 1985 Sep;163(3):1095-100
PMID: 2993233
-
Plasmids mediating iron uptake in Vibrio anguillarum strains isolated from turbot in Spain.
J Gen Microbiol. 1985 Aug;131(8):1989-97
PMID: 2997366
-
Studies on deo operon regulation in Escherichia coli: cloning and expression of the cytR structural gene.
Gene. 1985;36(1-2):37-44
PMID: 2998936
-
Characterization of anguibactin, a novel siderophore from Vibrio anguillarum 775(pJM1).
J Bacteriol. 1986 Jul;167(1):57-65
PMID: 3013839
-
Cloning and promoter identification of the iron-regulated cir gene of Escherichia coli.
J Bacteriol. 1987 Dec;169(12):5343-52
PMID: 3316180
-
Genetic and molecular characterization of essential components of the Vibrio anguillarum plasmid-mediated iron-transport system.
J Biol Chem. 1988 Feb 25;263(6):2853-60
PMID: 2830268
-
Genetic analysis of the iron uptake region of the Vibrio anguillarum plasmid pJM1: molecular cloning of genetic determinants encoding a novel trans activator of siderophore biosynthesis.
J Bacteriol. 1988 Apr;170(4):1913-9
PMID: 2832388
-
Chromosome-mediated iron uptake system in pathogenic strains of Vibrio anguillarum.
J Bacteriol. 1988 Apr;170(4):1920-5
PMID: 2965144
-
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):2110-4
PMID: 4559594