Abstract
We inserted the Tn10 tetracycline resistance determinant (tet) into the multicopy plasmid pACYC177, and we examined the phenotype of Escherichia coli K-12 strains harboring these plasmids. In agreement with others, we find that Tn10 tet exhibits a negative gene dosage effect. Strains carrying multicopy Tn10 tet plasmids are 4- to 12-fold less resistant to tetracycline than are strains with a single copy of Tn10 in the bacterial chromosome. In addition, we find that multicopy tet strains are 30- to 100-fold less resistant to the tetracycline derivative 5a,6-anhydrotetracycline than are single-copy tet strains. Multicopy tet strains are, in fact, 10- to 25-fold more sensitive to anhydrotetracycline than are strains that lack tet altogether. The hypersensitivity of multi-copy strains to anhydrotetracycline is correlated with the effectiveness of anhydrotetracycline as an inducer of tet gene expression, rather than its effectiveness as an inhibitor of protein synthesis. Anhydrotetracycline is 50- to 100-fold more effective than tetracycline as an inducer of tetracycline resistance and as an inducer of beta-galactosidase in strains that harbor tet-lac gene fusions. In contrast, anhydrotetracycline appears to be two- to fourfold less effective than tetracycline as an inhibitor of protein synthesis. Both anhydrotetracycline and tetracycline induce synthesis of tet polypeptides in minicells harboring multicopy tet plasmids. Differences between E. coli K-12 backgrounds influence the tetracycline and anhydrotetracycline sensitivity of multicopy strains; ZnCl2 enhances the tetracycline and anhydrotetracycline sensitivity of these strains two- to threefold. We propose that the overexpression of one or more Tn10 tet gene products inhibits the growth of multicopy tet strains and accounts for their relative sensitivity to inducers of tet gene expression.
MeSH Terms
Bacterial Proteins/biosynthesis
Chlorides
DNA Transposable Elements
Drug Resistance, Microbial
Escherichia coli/drug effects,genetics
Gene Expression Regulation
Genes, Bacterial
Plasmids
Tetracycline/pharmacology
Tetracyclines/pharmacology
Zinc/pharmacology
Zinc Compounds
beta-Galactosidase/genetics
Chemicals
Bacterial Proteins
Chlorides
DNA Transposable Elements
Tetracyclines
Zinc Compounds
4-epianhydrotetracycline
zinc chloride
beta-Galactosidase
Tetracycline
Zinc
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Moyed H S
Nguyen T T
Bertrand K P
References (30)
30 references, click to expand
-
Functional expression of cloned yeast DNA in Escherichia coli: specific complementation of argininosuccinate lyase (argH) mutations.
J Mol Biol. 1978 Apr 25;120(4):517-32
PMID: 349166
-
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature. 1970 Aug 15;227(5259):680-5
PMID: 5432063
-
Mutations in multicopy Tn10 tet plasmids that confer resistance to inhibitory effects of inducers of tet gene expression.
J Bacteriol. 1983 Aug;155(2):557-64
PMID: 6307969
-
Restriction enzyme cleavage map of Tn10, a transposon which encodes tetracycline resistance.
J Bacteriol. 1979 Jan;137(1):681-5
PMID: 762025
-
Specificity and mechanism of tetracycline resistance in a multiple drug resistant strain of Escherichia coli.
J Bacteriol. 1966 Feb;91(2):628-33
PMID: 5327360
-
Positive selection for loss of tetracycline resistance.
J Bacteriol. 1980 Aug;143(2):926-33
PMID: 6259126
-
Evidence for more than one mechanism of plasmid-determined tetracycline resistance in Escherichia coli.
J Gen Microbiol. 1980 Nov;121(1):221-9
PMID: 7019387
-
Translocation of the tetracycline resistance determinant from R100-1 to the Escherichia coli K-12 chromosome.
J Bacteriol. 1975 Dec;124(3):1153-8
PMID: 1104574
-
Generation of miniplasmids from copy number mutants of the R plasmid NR1.
J Bacteriol. 1977 Dec;132(3):986-95
PMID: 144723
-
Overlapping divergent promoters control expression of Tn10 tetracycline resistance.
Gene. 1983 Aug;23(2):149-56
PMID: 6311683
-
Plasmid-determined tetracycline resistance involves new transport systems for tetracycline.
Nature. 1978 Nov 2;276(5683):90-2
PMID: 368642
-
Analysis of the reduction in expression of tetracycline resistance determined by transposon Tn10 in the multicopy state.
Mol Gen Genet. 1981;182(1):171-7
PMID: 6267431
-
Identification of the tetracycline resistance promoter and repressor in transposon Tn10.
J Bacteriol. 1981 Aug;147(2):297-304
PMID: 6267006
-
Two complementation groups mediate tetracycline resistance determined by Tn10.
J Bacteriol. 1982 Jul;151(1):209-15
PMID: 6282805
-
Action of 12 tetracyclines on susceptible and resistant strains of Staphylococcus aureus.
Antimicrob Agents Chemother. 1973 Sep;4(3):237-47
PMID: 4758832
-
MINIATURE escherichia coli CELLS DEFICIENT IN DNA.
Proc Natl Acad Sci U S A. 1967 Feb;57(2):321-6
PMID: 16591472
-
Synthesis of ribonucleic acid and protein in plasmid-containing minicells of Escherichia coli K-12.
J Bacteriol. 1971 Jul;107(1):21-33
PMID: 4935321
-
Tetracycline resistance transposon Tn1721: recA-dependent gene amplification and expression of tetracycline resistance.
J Bacteriol. 1981 Sep;147(3):851-9
PMID: 6268611
-
Plasmid-mediated tetracycline resistance in Escherichia coli involves increased efflux of the antibiotic.
Biochem Biophys Res Commun. 1980 Mar 13;93(1):74-81
PMID: 6990931
-
Detection of an inducible membrane protein associated with R-factor-mediated tetracycline resistance.
Biochem Biophys Res Commun. 1974 Feb 27;56(4):1060-8
PMID: 4596957
-
A simple method for stabilizing protein-sulfhydryl groups during SDS-gel electrophoresis.
Anal Biochem. 1978 Jun 1;86(2):655-64
PMID: 655420
-
Replication control in a composite plasmid constructed by in vitro linkage of two distinct replicons.
Nature. 1976 Jan 29;259(5541):285-90
PMID: 765836
-
Reduced expression of Tn 10-mediated tetracycline resistance in Escherichia coli containing more than one copy of the transposon.
J Gen Microbiol. 1981 Sep;126(1):45-54
PMID: 6278056
-
Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid.
J Bacteriol. 1978 Jun;134(3):1141-56
PMID: 149110
-
Synthesis of an R plasmid protein associated with tetracycline resistance is negatively regulated.
Proc Natl Acad Sci U S A. 1976 May;73(5):1509-12
PMID: 775491
-
Organization of structural and regulatory genes that mediate tetracycline resistance in transposon Tn10.
J Bacteriol. 1979 Jun;138(3):705-14
PMID: 378932
-
Resistance of Escherichia coli to tetracyclines. Changes in permeability to tetracyclines in Escherichia coli bearing transferable resistance factors.
Biochem J. 1967 Oct;105(1):371-8
PMID: 4861886
-
Active efflux of tetracycline encoded by four genetically different tetracycline resistance determinants in Escherichia coli.
Proc Natl Acad Sci U S A. 1980 Jul;77(7):3974-7
PMID: 7001450
-
Selection for loss of tetracycline resistance by Escherichia coli.
J Bacteriol. 1981 Feb;145(2):1110-1
PMID: 7007341
-
A multifunctional gene (tetR) controls Tn10-encoded tetracycline resistance.
J Bacteriol. 1982 May;150(2):633-42
PMID: 6279565