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Anomalous expression of the E. coli lac operon in Proteus mirabilis

I. Effects of L8 and L8 UV5

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Summary

The lac operon shows anomalous expression in Proteus mirabilis: the maximal induced level is 10% or less of that in E. coli, while repression reduces this by a factor of only 2–5. We have sought to determine whether this effect relates in any way to CRP-mediated activation of expression, by comparing expression in P. mirabilis of lac operons (introduced for technical reasons on IncP1 plasmids) either regulatorily wild-type or bearing L8 or L8UV5. Derivatives of RP1 bearing L8UV5 were obtained by homogenotisation of pGC9114 (RP1:: Tn951) in a L8UV5 background; while derivatives of RP4 bearing lac +, L8 or L8UV5 were obtained by Mu-mediated translocation of chromosomal regions bearing these alleles, following partial heat-induction of Mucts62 on pGM14 (RP4:: Mucts62) in the appropriate hosts. These plasmids could be readily transferred to, and stably maintained in, the P. mirabilis strains employed. It was found that L8 reduced the maximal level of β-galactosidase activity, and L8UV5 restored this activity to around wild-type, in P. mirabilis quantitatively very much as in E. coli. Nevertheless, the low maximal level of expression and high basal level characteristic of the former host were unchanged. The simplest explanation of these results is that P. mirabilis contains a protein that mimics the E. coli CRP protein in interacting with the appropriate DNA binding site and thereby stimulating transcription; and that the anomalous regulation of lac in this host is unconnected with the CRP system.

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Abbreviations

CPR=:

cyclic AMP receptor protein

References

  • Baumberg S, Cornelis G, Panagiotakopoulos M, Roberts M (1980) Expression of the lactose transposon Tn951 in Escherichia coli, Proteus and Pseudomonas. J Gen Microbiol 119:257–262

    Google Scholar 

  • Baumberg S, Dennison S (1975) Variation in expression of sex factor genes in the Proteus-Providencia group relative to Escherichia coli. J Bacteriol 123:278–286

    Google Scholar 

  • Baumberg S, Roberts M (1984) Anomalous expression of the E. coli lac operon in Proteus mirabilis. II. Effects of lacI and lacP mutations. Mol Gen Genet 198:166–171

    Google Scholar 

  • Boucher B, Bergeron B, Barde de Bertalmio M, Dénarié J (1977) Introduction of bacteriophage Mu into Pseudomonas solanacearum and Rhizobium meliloti using the R factor RP4. J Gen Microbiol 98:253–263

    Google Scholar 

  • Burkhardt HJ, Riess G, Pühler A (1979) Relationship of group P1 plasmids revealed by heteroduplex experiments: RP1, RP4, R68 and RK2 are identical. J Gen Microbiol 114:341–348

    Google Scholar 

  • Colby C Jr, Hu ASL (1968a) The regulation of the synthesis of β-galactosidase in Proteus mirabilis F-lac. Biochim Biophys Acta 157:149–158

    Google Scholar 

  • Colby C Jr, Hu ASL (1968b) Purification and comparison of β-galactosidase synthesized by Escherichia coli F-lac + and Proteus mirabilis F-lac +. Biochim Biophys Acta 157:167–177

    Google Scholar 

  • Colby C Jr, Martin FD, Hu ASL (1968) Catabolite repression of the synthesis of β-galactosidase in Proteus mirabilis F-lac +. Biochim Biophys Acta 157:159–166

    Google Scholar 

  • Cone KC, Sellitti MA, Steege DA (1983) lac repressor mRNA transcription terminates in vivo in the lac control region. J Biol Chem 258:11296–11304

    Google Scholar 

  • Cornelis G, Ghosal D, Saedler H (1978) Tn951: a new transposon carrying a lactose operon. Mol Gen Genet 160:215–224

    Google Scholar 

  • Cozzarelli NR (1980) DNA gyrase and the supercoiling of DNA. Science 207:953–960

    Google Scholar 

  • Dale JW, Smith JT (1971) The purification and properties of the β-lactamase specified by the resistance factor R-1818 in Escherichia coli and Proteus mirabilis. Biochem J 123:493–500

    Google Scholar 

  • Dénarié J, Rosenberg C, Bergeron B, Boucher C, Michel M, Barde de Bertalmio M (1977) Potential of RP4:: Mu plasmid for in vivo genetic engineering of gram negative bacteria. In: Bukhari AI, Shapiro J, Adhya S (eds) DNA insertion elements, plasmids and episomes. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp 507–520

    Google Scholar 

  • Dennison S (1973) Control of fertility of resistance transfer factors in Proteus mirabilis and related bacterial species. Ph.D. thesis, University of Leeds

  • Dessein A, Schwartz M, Ullmann A (1978a) Catabolite repression in Escherichia coli mutants lacking cyclic AMP. Mol Gen Genet 162:83–87

    Google Scholar 

  • Dessein A, Tillier F, Ullmann A (1978b) Catabolite modulator factor: physiological properties and in vivo effects. Mol Gen Genet 162:89–94

    Google Scholar 

  • Faelen M, Toussaint A (1976) Bacteriophage Mu-1, a tool to transpose and to localize bacterial genes. J Mol Biol 104:525–539

    Google Scholar 

  • Falkow S, Wohlhieter JA, Citarella RV, Baron LS (1964) Transfer of episomic elements to Proteus. II. Nature of lac + Proteus strains isolated from clinical speciments. J Bacteriol 88:1598–1601

    Google Scholar 

  • Fried MG, Wu H-M, Crothers DM (1983) CAP binding to B and Z forms of DNA. Nucl Acids Res 11:2479–2494

    Google Scholar 

  • Gemski P Jr, Wohlhieter JA, Baron LS (1967) Chromosome transfer between Escherichia coli and Proteus mirabilis. Proc Natl Acad Sci USA 58:1461–1467

    Google Scholar 

  • Van Gijsegem F, Toussaint A, (1982) Chromosome transfer and R-prime formation by an RP4:: mini-Mu derivative in Escherichia coli, Salmonella typhimurium, Klebsiella pneumoniae, and Proteus mirabilis. Plasmid 7:30–44

    Google Scholar 

  • Glesyna ML, Bolshakova TN, Gershanovitch VN (1983) Effect of ptsI and ptsH mutations on initiation of transcription of the Escherichia coli lactose operon. Mol Gen Genet 190:417–420

    Google Scholar 

  • Greenblatt J, Li J, Adhya S, Friedman DI, Baron LS, Redfield B, Kung H-F, Weissbach H (1980) L factor that is required for β-galactosidase synthesis is the nusA gene product involved in transcription termination. Proc Natl Acad Sci USA 77:1991–1994

    Google Scholar 

  • Guidi-Rontani C, Danchin A, Ullmann A (1980) Catabolite repression in Escherichia coli mutants lacking cyclic AMP receptor protein. Proc Natl Acad Sci USA 77:1991–1994

    Google Scholar 

  • Kolb A, Buc H (1982) Is DNA unwound by the cyclic AMP receptor protein? Nucl Acids Res 10:473–485

    Google Scholar 

  • Low B (1972) Escherichia coli K-12 F-prime factors, old and new. Bacteriol Rev 36:587–607

    Google Scholar 

  • McKay DB, Steitz TA (1981) Structure of catabolite gene activator protein at 2.9 Å resolution suggests binding to left-handed B-DNA. Nature 290:744–749

    Google Scholar 

  • Manson MD, Yanofsky C (1976) Tryptophan operon regulation in interspecific hybrids of enteric bacteria. J Bacteriol 126:679–689

    Google Scholar 

  • Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York

    Google Scholar 

  • Morgan EA, Kaplan S (1976) Transcription of Escherichia coli ribosomal DNA in Proteus mirabilis. Mol Gen Genet 147:179–188

    Google Scholar 

  • Morgan EA, Kaplan S (1977) Expression and stability of Escherichia coli F-prime factors in Proteus mirabilis. Mol Gen Genet 151:41–47

    Google Scholar 

  • Pribnow D (1979) Genetic control signals in DNA. In: Goldberger RF (ed) Biological regulation and development, vol 1. Gene expression. Plenum, New York, pp 219–278

    Google Scholar 

  • Primakoff P, Artz SW (1979) Positive control of lac operon expression in vitro by guanosine 5′-diphosphate 3′-diphosphate. Proc Natl Acad Sci USA 76:1726–1730

    Google Scholar 

  • Reznikoff WS, Abelson JN (1980) The lac promoter. In: Miller JH, Reznikoff WS (eds) The operon (2nd ed). Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp 221–243

    Google Scholar 

  • Roberts M (1982) Studies on the mechanism of anomalous expression of foreign genes in Proteus mirabilis. Ph.D.thesis, University of Leeds

  • Sanzey B (1979) Modulation of gene expression by drugs affecting deoxyribonucleic acid gyrase. J Bacteriol 138:40–47

    Google Scholar 

  • Sanzey B, Ullmann A (1980) The effect of urea on catabolite sensitive operons in Escherichia coli K 12. Mol Gen Genet 178:611–616

    Google Scholar 

  • Silverstone AE, Arditti RR, Magasanik B (1970) Catabolite-insensitive revertants of lac promoter mutations. Proc Natl Acad Sci USA 66:773–776

    Google Scholar 

  • Smith JT (1969) R-factor expression in Gram-negative bacteria. J Gen Microbiol 55:109–120

    Google Scholar 

  • Stubbs J, Horwitz A, Moses V (1973) Studies on β-galactoside transport in a Proteus mirabilis merodiploid carrying an Escherichia coli lactose operon. J Bacteriol 116:131–140

    Google Scholar 

  • Ullmann A, Danchin A (1983) Role of cyclic AMP in bacteria. Adv Cylic Nucleotide Res 15:1–53

    Google Scholar 

  • Ullmann A, Tillier F, Monod J (1976) Catabolite modulator factor: a possible mediator of catabolite repression in bacteria. Proc Natl Acad Sci USA 73:3476–3479

    Google Scholar 

  • Ullmann A, Joseph E, Danchin A (1979) Cyclic AMP as a modulator of polarity in polycistronic transcriptional units. Proc Natl Acad Sci USA 76:3194–3197

    Google Scholar 

  • Wohlhieter J, Falkow S, Citarella RV, Baron LS (1964) Characterization of DNA from a Proteus strain harboring an episome. J Mol Biol 9:576–588

    Google Scholar 

  • Wohlhieter JA, Gemski P Jr, Baron LS (1975) Extensive segments of the Escherichia coli K12 chromosome in Proteus mirabilis diploids. Mol Gen Genet 139:93–101

    Google Scholar 

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Author notes

  1. Margo Roberts

    Present address: Laboratoire de Génétique Moléculaire des Eucaryotes du CNRS, Unité 184 de l'INSERM, Institut de Chimie Biologique, Faculté de Médecine, Strasbourg, France

Authors and Affiliations

  1. Department of Genetics, University of Leeds, LS2 9JT, Leeds, UK

    Margo Roberts & Simon Baumberg

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  1. Margo Roberts
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  2. Simon Baumberg
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Communicated by C. Auerbach

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Roberts, M., Baumberg, S. Anomalous expression of the E. coli lac operon in Proteus mirabilis . Molec Gen Genet 198, 159–165 (1984). https://doi.org/10.1007/BF00328716

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