Genetic analysis of a plasmid-encoded, host genotype-specific enhancement of bacterial fitness

In the absence of antibiotics, carriage of pACYC184 reduces the competitive fitness of an Escherichia coli B genotype that was not previously selected for plasmid carriage, relative to that of an isogenic plasmid-free competitor. However, a host genotype propagated with the plasmid for 500 generations evolved an unexpected competitive advantage from plasmid carriage, relative to its own isogenic plasmid-free segregant. We manipulated the pACYC184 genome in order to identify the plasmid-encoded function that was required for the enhancement of the coevolved host genotype's competitive fitness. Inactivation of the plasmid-encoded tetracycline resistance gene, by deletion of either the promoter region or the entire gene, eliminated the beneficial effect of plasmid carriage for the coevolved host. This beneficial effect for the coevolved host was also manifest with pBR322, which contains a tetracycline resistance gene identical to that of pACYC184 but is otherwise heterologous.

[1]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[2]  H. Marešová,et al.  Plasmid burden in chemostat culture of Escherichia coli: Its effect on the selection for overproducers of host enzymes , 1993, Biotechnology and bioengineering.

[3]  J. Adams,et al.  The ecology and evolution of tetracycline resistance. , 1992, Trends in ecology & evolution.

[4]  Mitchell L. Cohen Epidemiology of Drug Resistance: Implications for a Post—Antimicrobial Era , 1992, Science.

[5]  H. Neu,et al.  The Crisis in Antibiotic Resistance , 1992, Science.

[6]  John E Mittler,et al.  EVOLUTIONARY ADAPTATION TO TEMPERATURE. I. FITNESS RESPONSES OF ESCHERICHIA COLI TO CHANGES IN ITS THERMAL ENVIRONMENT , 1992, Evolution; international journal of organic evolution.

[7]  R. Lenski,et al.  Long-Term Experimental Evolution in Escherichia coli. I. Adaptation and Divergence During 2,000 Generations , 1991, The American Naturalist.

[8]  W. Arber,et al.  Bleomycin-resistance gene derived from the transposon Tn5 confers selective advantage to Escherichia coli K-12. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[9]  K. Kam,et al.  BsiY I, a novel thermophilic restriction endonuclease that recognizes 5' CCNNNNNNNGG 3' and the discovery of a wrongly sequenced site in pACYC177. , 1991, Nucleic acids research.

[10]  C. Beck,et al.  Overproduction of transposon Tn10-encoded tetracycline resistance protein results in cell death and loss of membrane potential , 1989, Journal of bacteriology.

[11]  R. Lenski,et al.  Effects of carriage and expression of the Tn10 tetracycline-resistance operon on the fitness of Escherichia coli K12. , 1989, Molecular biology and evolution.

[12]  N. Watson A new revision of the sequence of plasmid pBR322. , 1988, Gene.

[13]  J. E. Bouma,et al.  Evolution of a bacteria/plasmid association , 1988, Nature.

[14]  R. Lenski EXPERIMENTAL STUDIES OF PLEIOTROPY AND EPISTASIS IN ESCHERICHIA COLI. II. COMPENSATION FOR MALADAPTIVE EFFECTS ASSOCIATED WITH RESISTANCE TO VIRUS T4 , 1988, Evolution; international journal of organic evolution.

[15]  R. Lenski EXPERIMENTAL STUDIES OF PLEIOTROPY AND EPISTASIS IN ESCHERICHIA COLI. I. VARIATION IN COMPETITIVE FITNESS AMONG MUTANTS RESISTANT TO VIRUS T4 , 1988, Evolution; international journal of organic evolution.

[16]  R. Lenski,et al.  Stability of recombinant DNA and its effects on fitness. , 1988, Trends in ecology & evolution.

[17]  R. E. Rose,et al.  The nucleotide sequence of pACYC184 , 1988, Nucleic Acids Res..

[18]  Richard P. Novick,et al.  Antibiotic Resistance Genes: Ecology, Transfer, and Expression , 1987 .

[19]  J. Stephenson,et al.  The insertion of large pieces of foreign genetic material reduces the stability of bacterial plasmids. , 1986, Plasmid.

[20]  K. Backman In vivo events in the generation of pBR322. , 1986, Nucleic Acids Research.

[21]  J. Bailey,et al.  Effects of recombinant plasmid content on growth properties and cloned gene product formation in Escherichia coli , 1985, Biotechnology and bioengineering.

[22]  R. Lenski,et al.  Constraints on the Coevolution of Bacteria and Virulent Phage: A Model, Some Experiments, and Predictions for Natural Communities , 1985, The American Naturalist.

[23]  R. Siegel,et al.  Kinetic study of instability of recombinant plasmid pPLc23trpAl in E. coli using two‐stage continuous culture system , 1985, Biotechnology and bioengineering.

[24]  D. Dosch,et al.  Tetracycline resistance element of pBR322 mediates potassium transport , 1984, Journal of bacteriology.

[25]  R. Rodriguez,et al.  A Bacteriophage λ Cohesive Ends (cos) DNA Fragment Enhances the Fitness of Plasmid-Containing Bacteria Growing in Energy-Limited Chemostats , 1984, Bio/Technology.

[26]  D. Hartl,et al.  Transposable element IS50 improves growth rate of E. coli cells without transposition , 1983, Cell.

[27]  T. Nguyen,et al.  Multicopy Tn10 tet plasmids confer sensitivity to induction of tet gene expression , 1983, Journal of bacteriology.

[28]  H. Moyed,et al.  Mutations in multicopy Tn10 tet plasmids that confer resistance to inhibitory effects of inducers of tet gene expression , 1983, Journal of bacteriology.

[29]  D. Hartl,et al.  Selection in chemostats. , 1983, Microbiological reviews.

[30]  D. Hartl,et al.  Evolution of transposons: natural selection for Tn5 in Escherichia coli K12. , 1983, Genetics.

[31]  J. A. Mckenzie,et al.  The effect of genetic background on the fitness of diazinon resistance genotypes of the Australian sheep blowfly, Lucilia cuprina , 1982, Heredity.

[32]  R. A. Walters,et al.  Plasmid-conferred tetracycline resistance confers collateral cadmium sensitivity of E. coli cells. , 1982, Plasmid.

[33]  Dm Jones,et al.  Fundamentals of Oncology , 1981 .

[34]  J. Adams,et al.  The maintenance of Plasmid-containing organisms in populations of Escherichia coli. , 1981, Journal of general microbiology.

[35]  Stanley Maloy,et al.  Selection for loss of tetracycline resistance by Escherichia coli , 1981, Journal of bacteriology.

[36]  B. Ames,et al.  Positive selection for loss of tetracycline resistance , 1980, Journal of bacteriology.

[37]  S. Levy,et al.  Active efflux of tetracycline encoded by four genetically different tetracycline resistance determinants in Escherichia coli. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[38]  S. Levy,et al.  Heterogeneity of tetracycline resistance determinants. , 1980, Plasmid.

[39]  J. H. Slater,et al.  The influence of the growth environment on the stability of a drug resistance plasmid in Escherichia coli K12. , 1979, Journal of general microbiology.

[40]  A. C. Chang,et al.  Revised Interpretation of the Origin of the pSC101 Plasmid , 1977, Journal of bacteriology.

[41]  F. M. Stewart,et al.  A Complex Community in a Simple Habitat: An Experimental Study with Bacteria and Phage , 1977 .

[42]  L. Lin,et al.  Increased reproductive fitness of Escherichia coli lambda lysogens , 1977, Journal of virology.

[43]  F. M. Stewart,et al.  Resource-Limited Growth, Competition, and Predation: A Model and Experimental Studies with Bacteria and Bacteriophage , 1977, The American Naturalist.

[44]  H. Smith,et al.  Persistence of tetracycline resistance in pig E. coli , 1975, Nature.

[45]  R. Kudrna,et al.  λ Lysogens of E. coli reproduce more rapidly than non-lysogens , 1975, Nature.

[46]  R. Lenski Quantifying fitness and gene stability in microorganisms. , 1991, Biotechnology.

[47]  James J. Barondess,et al.  A bacterial virulence determinant encoded by lysogenic coliphage λ , 1990, Nature.

[48]  G. Edlin,et al.  Expression of tetracycline resistance in pBR322 derivatives reduces the reproductive fitness of plasmid-containing Escherichia coli. , 1985, Gene.

[49]  L. Runkel,et al.  THE NUCLEOTIDE SEQUENCE OF pACYC 177 , 1982 .

[50]  B. Levin Conditions for the Existence of R-Plasmids in Bacterial Populations , 1980 .

[51]  G. Lebek,et al.  Generation time-prolonging R plasmids: correlation between increases in the generation time of Escherichia coli caused by R plasmids and their molecular size. , 1980, Plasmid.

[52]  J. Sutcliffe Complete nucleotide sequence of the Escherichia coli plasmid pBR322. , 1979, Cold Spring Harbor symposia on quantitative biology.

[53]  H. Smith Persistence of tetracycline resistance in pig. , 1975 .

[54]  S. Falkow Infectious multiple drug resistance , 1975 .