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On the evolution of Tn21-like multiresistance transposons: Sequence analysis of the gene (aacC1) for gentamicin acetyltransferase-3-I(AAC(3)-I), another member of the Tn21-based expression cassette

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Summary

The aminoglycoside-3-O-acetyltransferase-I gene (aacC1) from R plasmids of two incompatibility groups (R1033 [Tn1696], and R135) was cloned and sequenced. In the case of R1033, it was shown that theaacC gene is coded by a precise insertion of 833 bp between theaadA promoter and its structural gene in a Tn21 related transposon (Tn1696). This insertion occurs at the same target sequence as that of the OXA-1 β-lactamase gene insertion in Tn2603. Upstream of theaacC gene, we found an open reading frame (ORF) which is probably implicated in the site-specific recombinational events involved in the evolution of this family of genetic elements. These results provide additional confirmation of the role of Tn21 elements as naturally occurring interspecific transposition and expression casssettes.

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References

  • Allmansberger R, Bräu B, Piepersberg W (1985) Genes for gentamicin-(3)-N-acetyl-transferases III and IV: II. Nucleotide sequences of three AAC(3)-III genes and evolutionary aspects. Mol Gen Genet 198:514–520

    Article  PubMed  CAS  Google Scholar 

  • Bräu B, Pilz U, Piepersberg W (1984) Genes for gentamicin-(3)-N-acetyltransferases III and IV. I. Nucleotide sequence of the AAC(3)-IV gene and possible involvement of an IS140 element in its expression. Mol Gen Genet 193:179–187

    Article  PubMed  Google Scholar 

  • Brzezniska M, Benveniste R, Davies J, Daniels PJL, Weinstein J (1972) Gentamicin resistance in strains ofPseudomonas aeruginosa mediated by enzymatic N-acetylation of the 2-deoxystreptamine moiety. Biochemistry 11:761–766

    Article  Google Scholar 

  • Cameron FH, Groot Obbink DJ., Ackerman VP, Hall RM (1986) Nucleotide sequence of the AAD(2″) aminoglycoside adenylyltransferase determinantaadB. Evolutionary relationship of this region with those surroundingaadA in R538-1 anddhfrII in R388. Nucleic Acids Res 14:8625–8635

    PubMed  CAS  Google Scholar 

  • Chinault AC, Blakesley VA, Roessler E, Willis DG, Smith CA, Cook RG, Fenwick RG jr (1986) Characterisation of transferable plasmids fromShigella flexneri 2a that confer resistance to trimethoprim, streptomycin, and sulfonamides. Plasmid 15:119–131

    Article  PubMed  CAS  Google Scholar 

  • Davies J (1986a) A new look at antibiotic resistance. FEMS Microbiol Revs 39:363–371

    Article  CAS  Google Scholar 

  • Davies JE (1986b) Aminoglycoside-aminocyclitol antibiotics and their modifying enzymes. In: Antibiotics in laboratory medicine, Second edition. Williams & Wilkins, Baltimore, pp 790–809

    Google Scholar 

  • Davies J, Smith DI (1978) Plasmid determined resistance to antimicrobial agents. Annu Rev Microbiol 32:469–518

    Article  PubMed  CAS  Google Scholar 

  • De la Cruz F, Grinsted J (1982) Genetic and molecular characterisation of Tn21, a multiple resistance transposon from R100-1. J Bacteriol 151:222–228

    PubMed  Google Scholar 

  • Dowding J, Davies J (1975) Mechanisms and origins of plasmid-determined antibiotic resistance. Microbiology 1974. American Soc Microbiol, Washington DC, pp 179–186

    Google Scholar 

  • Flensburg J, Steen R (1986) Nucleotide sequence analysis of the trimethoprim resistant dihydrofolate reductase encoded by R plasmid R751. Nucleic Acids Res 14:5933

    PubMed  CAS  Google Scholar 

  • Fling ME, Kopf J, Richards C (1985) Nucleotide sequence of the transposon Tn7 gene encoding an aminoglycoside-modifying enzyme, 3″(9)-O-nucleotidyltransferase. Nucleic Acids Res 13:7095–7106

    PubMed  CAS  Google Scholar 

  • Haas MJ, Dowding JE (1975) Aminoglycoside-modifying enzymes. Methods Enzymol 43:611–640

    Article  PubMed  CAS  Google Scholar 

  • Hall RM, Vockler C (1987) The region of the IncN plasmid R46 coding for resistance to β-lactam antibiotics, streptomycin/spectinomycin and sulphonamides is closely related to antibiotic resistance segments found in IncW plasmids and in Tn21-like transposons. Nucleic Acids Res 15:7491–7501

    PubMed  CAS  Google Scholar 

  • Hirsch PR, Beringer JE (1984) A physical map of pPH1J1 and pJB4J1. Plasmid 12:139–141

    Article  PubMed  CAS  Google Scholar 

  • Hirsch PR, Wang CL, Woodward MJ (1986) Construction of a Tn5 derivative determining resistance to gentamicin and spectinomycin using a fragment cloned from R1033. Gene 48:203–209

    Article  PubMed  CAS  Google Scholar 

  • Hollingshead S, Vapnek D (1985) Nucleotide sequence analysis of a gene encoding a streptomycin/spectinomycin adenyltransferase. Plasmid 13:17–30

    Article  PubMed  CAS  Google Scholar 

  • Hsiang MW, White TJ, Davies JE (1978) NH2-terminal sequence of the aminoglycoside acetyltransferase (3)-I mediated by plasmid RIP135. FEBS Lett 92:97–99

    Article  PubMed  CAS  Google Scholar 

  • Huovinen P, Huovinen S, Jacoby GA (1988) Sequence of PSE-2 β-lactamase. Antimicrob Agents Chemother 32:134–136

    PubMed  CAS  Google Scholar 

  • Kagan SA (1981) Aminoglycoside acetyltransferase-3-I; structure and function. Ph.D. Thesis, University of Wisconsin

  • Kagan SA, Davies JE (1980) Enzymatic modification of aminoglycoside antibiotics: mutations affecting the expression of aminoglycoside acetyltransferase-3. Plasmid 3:312–318

    Article  PubMed  CAS  Google Scholar 

  • Lafond M, Couture F, Vezina G, Levesque RC (1989) DNA homology, structural features and evolutionary perspectives of multiresistance complex β-lactamase transposons. (In press)

  • LeGoffic F, Moreau N (1973) Purification by affinity chromatography of an enzyme involved in gentamicin inactivation. FEBS Lett 29:289–291

    Article  CAS  Google Scholar 

  • LeGoffic F, Martel A, Witchitz J (1974) 3-N-enzymatic acetylation of gentamicin, tobramycin and kanamycin byEscherichia coli carrying an R-factor. Antimicrob Agents Chemother 6:680–684

    CAS  Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular Cloning. Cold Spring Harbor Laboratory

  • Marti KM (1987) Kinetic characterisation of aminoglycoside acetyltransferase 3-1. Ph.D. Thesis, University of Wisconsin

  • Martinez E, de la Cruz F (1988) Transposon Tn21 encodes arecA-independent site-specific integration system. Mol Gen Genet 211:320–325

    Article  PubMed  CAS  Google Scholar 

  • Mitsuhashi S (1982) Antibacterial activity of aminoglycoside antibiotics. In: Umezawa H, Hooper IR (eds) Aminoglycoside Antibiotics. Springer-Verlag, Berlin, pp 205–220

    Google Scholar 

  • Ouellette M, Roy PH (1986) Analysis by DNA probes of the OXA-1 β-lactamase gene and its transposon. Antimicrob Agents Chemother 30:46–51

    PubMed  CAS  Google Scholar 

  • Ouellette M, Roy PH (1987) Homology of ORFs from Tn2603 and from R46 to site-specific recombinases. Nucleic Acids Res 15:10055–10056

    PubMed  CAS  Google Scholar 

  • Ouellette M, Bissonnette L, Roy PH (1987) Precise insertion of antibiotic resistance determinants into Tn21-like transposons: Nucleotide sequence of the OXA-1 β-lactamase gene. Proc Natl Acad Sci USA 84:7378–7382

    Article  PubMed  CAS  Google Scholar 

  • Piepersberg W, Distler J, Heinzel P, Perez-Gonzalez J-A (1988) Antibiotic resistance by modification: many resistance genes could be derived from cellular control genes in Actinomycetes — a hypothesis. Actinomycetologica, in press

  • Pratt JM (1984) Coupled transcription-translation in prokaryotic cell-free systems. In: Hames BD, Higgins SJ(eds) Transcription and translation: A practical approach. IRL Press, Oxford, pp 179–209

    Google Scholar 

  • Rubens CE, McNeill WF, Farrer WE (1979) A transposable plasmid DNA sequence inPseudomonas aeruginosa which mediates resistance to gentamicin and four other antibiotics. J Bacteriol 139:877–882

    PubMed  CAS  Google Scholar 

  • Rubin RA (1987) Genetic analysis of the gentamicin resistance region of pPH1J1 and incorporation into a wide host range cloning vehicle. Plasmid 18:84–88

    Article  PubMed  CAS  Google Scholar 

  • Schmidt F (1984) The role of insertions, deletions, and substitutions in the evolution of R6 related plasmids encoding aminoglycoside transferase ANT-(2″). Mol Gen Genet 194:248–259

    Article  PubMed  CAS  Google Scholar 

  • Schmidt F, Klopfer-Kaul I (1984) Evolutionary relationship between Tn21-like elements and pBP201, a plasmid fromKlebsiella pneumoniae mediating resistance to gentamicin and eight other drugs. Mol Gen Genet 197:109–119

    Article  PubMed  CAS  Google Scholar 

  • Simonsen CC, Chen EY, Levinson AD (1983) Identification of the type I trimethoprim-resistant dihydrofolate reductase specified by theEscherichia coli R-plasmid R483: comparison with procaryotic and eucaryotic dihydrofolate reductases. J Bacteriol 155:1001–1008

    PubMed  CAS  Google Scholar 

  • Smith DI, Gomez Lus R, Rubio Calvo M, Datta N, Jacob AE, Hedges RW (1975) Third type of plasmid conferring gentamicin resistance inPseudomonas aeruginosa. Antimicrob Agents Chemother 8:227–230

    PubMed  CAS  Google Scholar 

  • Sundström L, Rådström P, Swedberg G, Sköld O (1988) Site-specific recombination promotes linkage between trimethoprimand sulfonamide resistance genes. Sequence characterization ofdhfrV andsulI and a recombination active locus of Tn21. Mol Gen Genet 213:191–201

    Article  PubMed  Google Scholar 

  • Swift G, McCarthy BJ, Heffron F (1981) DNA sequence of a plasmid-encoded dihydrofolate reductase. Mol Gen Genet 181:441–447

    Article  PubMed  CAS  Google Scholar 

  • Tait RC, Rempel H, Rodriguez RL, Kado CI (1985) The aminoglycoside resistance operon of the plasmid pSa: Nucleotide sequence of the streptomycin/spectinomycin resistance gene. Gene 36:97–104

    Article  PubMed  CAS  Google Scholar 

  • Tanaka M, Matshushita K, Yamamoto T (1985) Genesis of a complex transposon encoding the OXA-1 (type II) β-lactamase gene. Antimicrob Agents Chemother 28:227–234

    PubMed  CAS  Google Scholar 

  • Tenover FC, Filpula D, Phillips KL, Plorde JJ (1988) Cloning and sequencing of a gene encoding an aminoglycoside 6′-N-acetyltransferase from an R factor ofCitrobacter diversus. J Bacteriol 170:471–473

    PubMed  CAS  Google Scholar 

  • Umezawa H, Yagisawa M, Matsuhashi Y, Nagenawa H, Yamamoto H, Kondo S, Takenchi T, Chabbert YA (1973) Gentamicin acetyltransferase inEscherichia coli carrying R factor. J Antibiot 26:612–614

    PubMed  CAS  Google Scholar 

  • Wiedemann B, Meyer JF, Zuhlsdorf M (1987) Insertions of resistance genes into Tn21-like transposons. J Antimicrob Chemother 18:85–92

    Google Scholar 

  • Williams JW, Northrop DB (1976) Purification and properties of gentamicin acetyltransferase I. Biochemistry 15:125–131

    Article  PubMed  CAS  Google Scholar 

  • Williams JW, Northrop DB (1978a) Kinetic mechanisms of gentamicin acetyltransferase I. Biol Chem 253:5902–5907

    CAS  Google Scholar 

  • Williams JW, Northrop DB (1978b) Substrate specificity and structure-activity relationships of gentamicin acetyltransferase I. J Biol Chem 253:5908–5914

    PubMed  CAS  Google Scholar 

  • Witchitz JL (1972) Plasmid-mediated gentamicin resistance not associated with kanamycin resistance in Enterobacteriaceae. J Antibiot 25:622–624

    PubMed  CAS  Google Scholar 

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Author notes

  1. Sarah A. Kagan

    Present address: Banner, Birch, McKie & Beckett, Thomas Circle, NW, 20005, Washington, DC, USA

Authors and Affiliations

  1. Fakultät für Biologie, Universität Bielefeld, 4800, Bielefeld 1, Federal Republic of Germany

    Wolfgang Wohlleben & Walter Arnold

  2. Université Laval, GIV 4G2, Sainte-Foy, Quebec, Canada

    Luc Bissonnette, Alex Pelletier, Annie Tanguay & Paul H. Roy

  3. Monsanto Company, 63198, St. Louis, Missouri, USA

    Gary C. Gamboa & Gerard F. Barry

  4. Institut Pasteur, F-75724, Paris, Cedex 15, France

    Elisabeth Aubert, Julian Davies & Sarah A. Kagan

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  1. Wolfgang Wohlleben
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  2. Walter Arnold
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Communicated by W. Arber

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Wohlleben, W., Arnold, W., Bissonnette, L. et al. On the evolution of Tn21-like multiresistance transposons: Sequence analysis of the gene (aacC1) for gentamicin acetyltransferase-3-I(AAC(3)-I), another member of the Tn21-based expression cassette. Molec. Gen. Genet. 217, 202–208 (1989). https://doi.org/10.1007/BF02464882

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  • DOI: https://doi.org/10.1007/BF02464882

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