Molecular and General Genetics MGG

, Volume 205, Issue 2, pp 291–297 | Cite as

Transposable multiple antibiotic resistance in Streptococcus pneumoniae

  • Patrice Courvalin
  • Cécile Carlier
Article

Summary

A mobile genetic element, designated Tn1545, was detected in the chromosome of Streptococcus pneumoniae BM4200, a clinical isolate multiply resistant to antibiotics. The 25.3 kb element conferred resistance to kanamycin and structurally related aminoglycosides by synthesis of a 3′-aminoglycoside phosphotranferase type III (aphA-3), to macrolide-lincosamide-streptogramin B-type antibiotics (ermAM), and to tetracycline (tetM). Tn1545 was self-transferable to a recombination deficient S. faecalis strain where it was able to transpose to various sites, induce insertional mutations and was apparently cleanly excised. The element also conjugated to and transposed to the chromosome of S. faecalis, S. lactis, S. diacetylactis, S. cremoris, S. sanguis, Staphylococcus aureus, and Listeria monocytogenes. The properties of the conjugative transposon Tn1545 could account for the sudden emergence, rapid dissemination, and stabilisation of multiple resistance to antibiotics in S. pneumoniae in the absence of plasmids.

Key words

Pneumococcus Antibiotic resistance Conjugative transposon 

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References

  1. Borderon E, Bieth G, Horodniceanu T (1982) Genetic and physical studies of Streptococcus faecalis hemolysin plasmids. FEMS Microbiol Lett 14:51–55Google Scholar
  2. Boyer HW, Roulland-Dussoix D (1969) A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol 41:459–472Google Scholar
  3. Burdett V, Inamine J, Rajagopalan S (1982) Multiple tetracycline resistance determinants in Streptococcus. In: Schlessinger D (ed) Microbiology-1982. American Society for Microbiology, Washington DC, pp 155–158Google Scholar
  4. Buu-Hoï A, Horodniceanu T (1980) Conjugative transfer of multiple antibiotic resistance markers in Streptococcus pneumoniae. J Bacteriol 143:313–320Google Scholar
  5. Carlier C, Courvalin P (1982a) Resistance of streptococci to aminoglycoside-aminocyclitol antibiotics. In: Schlessinger D (ed) Microbiology-1982. American Society for Microbiology, Washington DC, pp 162–166Google Scholar
  6. Carlier C, Courvalin P (1982b) A plasmid which does not encode the aminoglycoside phosphotransferase in the butirosin-producing strain of Bacillus circulans. J Antibiot 35:629–634Google Scholar
  7. Clewell DB (1981) Plasmids drug resistance, and gene transfer in the genus Streptococcus. Microbiol Rev 45:409–436Google Scholar
  8. Collatz E, Carlier C, Courvalin P (1983) The chromosomal 3′5″-aminoglycoside phosphotransferase in Streptococcus pneumoniae is closely related to its plasmid-coded homologues in Streptococcus faecalis and Staphylococcus aureus. J Bacteriol 156:1373–1377Google Scholar
  9. Collatz E, Carlier C, Courvalin P (1984) Characterization of highlevel aminoglycoside resistance in a strain of Streptococcus pneumoniae. J Gen Microbiol 130:1665–1671Google Scholar
  10. Courvalin P, Carlier C (1987) Tn1545: A conjugative shuttle transposon. Mol Gen Genet (in press)Google Scholar
  11. Courvalin P, Davies J (1977) Plasmid-mediated aminoglycoside phosphotransferase of broad substrate range that phosphorylates amikacin. Antimicrob Agents Chemother 11:619–624Google Scholar
  12. Courvalin P, Fiandt M (1980) Aminoglycoside-modifying enzymes of Staphylococcus aureus: expression in Escherichia coli. Gene 9:247–269Google Scholar
  13. Courvalin PM, Carlier C, Chabbert YA (1972) Plasmid-linked tetracycline and erythromycin resistance in group D “Streptococcus”. Ann Inst Pasteur (Paris) 123:755–759Google Scholar
  14. Courvalin PM, Shaw WV, Jacob AE (1978) Plasmid-mediated mechanisms of resistance to aminoglycoside antibiotics and to chloramphenicol in group D streptococci. Antimicrob Agents Chemother 13:716–725Google Scholar
  15. Courvalin P, Carlier C, Collatz E (1979) Structural and functional relationships between plasmid-mediated aminocyclitol-modifying enzymes from Gram-positive and Gram-negative bacteria. Program abstract no. 85, 11th Lunteren Lecture, Lunteren, The NetherlandsGoogle Scholar
  16. Courvalin P, Carlier C, Collatz E (1980) Plasmid-mediated resistance to aminocyclitol antibiotics in group D streptococci. J Bacteriol 143:541–551Google Scholar
  17. Cross-Belard M, Oudet P, Chambon P (1973) Isolation of high molecular weight DNA from mammalian cells. Eur J Biochem 36:32–38Google Scholar
  18. Denhardt DT (1966) A membrane filter technique for the detection of complementary DNA. Biochem Biophys Res Commun 23:641–646Google Scholar
  19. Engel HWB, Soedirman N, Rost JA, van Leeuwen WJ, van Embden JDA (1980) Transferability of macrolide, lincomycin, and streptogramin resistances between group A, B, and D streptococci. Streptococcus pneumoniae, and Staphylococcus aureus. J Bacteriol 142:407–413Google Scholar
  20. Fitzgerald GF, Clewell DB (1985) A conjugative transposon (Tn919) in Streptococcus sanguis. Infect Immun 47:415–420Google Scholar
  21. Franke AE, Clewell DB (1981) Evidence for a chromosome-borne resistance transposon (Tn916) in Streptococcus faecalis that is capable of “conjugal” tranfer in the absence of a conjugative plasmid. J Bacteriol 145:494–502Google Scholar
  22. Gaillard JL, Berche P, Sansonetti P (1986) Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes. Infect Immun 52:50–55Google Scholar
  23. Gawron-Burke C, Clewell DB (1984) Regeneration of insertionally inactivated streptococcal DNA fragments after excision of Tn916 in Escherichia coli: strategy for targeting and cloning of genes from gram-positive bacteria. J Bacteriol 159:214–221Google Scholar
  24. Guild WR, Smith MD, Shoemaker NB (1982) Conjugative transfer of chromosomal R determinants in Streptococcus pneumoniae. In: Schlessinger D (ed) Microbiology-1982. American Society for Microbiology, Washington DC, pp 88–92Google Scholar
  25. Haas MJ, Dowding JE (1975) Aminoglycoside-modifying enzymes. Methods Enzymol 43:611–628Google Scholar
  26. Jacob AE, Hobbs SJ (1974) Conjugal transfer of plasmid-borne multiple antibiotic resistance in Streptococcus faecalis var. zymogenes. J Bacteriol 117:360–372Google Scholar
  27. Jacobs MR, Koornhof HJ, Robins-Browne RM, Stevenson CM, Freiman I, Miller GB, Witcomb MA, Isaacson M, Ward JI, Austrian R (1978) Emergence of multiply resistant pneumonocci. N Engl J Med 299:735–740Google Scholar
  28. Lambert T, Gerbaud G, Trieu-Cuot P, Courvalin P (1985) Structural relationship between the genes encoding 3′-aminoglycoside phosphotransferases type III from Campylobacter and Gram-positive cocci. Ann Microbiol Inst Pasteur (Paris) 136B:135–150Google Scholar
  29. Lederberg EM (1981) Plasmid reference center registry of transposon (Tn) allocations through July 1981. Gene 16:59–61Google Scholar
  30. Lereclus D, Menou G, Lecadet MM (1983) Isolation of a DNA sequence related to several plasmids from Bacillus thuringiensis after mating involving the Streptococcus faecalis plasmid pAMβ1. Mol Gen Genet 191:307–313Google Scholar
  31. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory. Cold Spring Harbor, NYGoogle Scholar
  32. Maniatis T, Jeffrey A, Kleid DG (1975) Nucleotide sequence of the rightward operator of phage λ. Proc Natl Acad Sci USA 72:1184–1188Google Scholar
  33. Martin P, Trieu-Cuot P, Courvalin P (1986) Nucleotide sequence of the tetM tetracycline resistance determinant of the streptococcol conjugative shuttle transposon Tn1545. Nucl Acids Res 17:7047–7058Google Scholar
  34. Novick RP, Clowes RC, Cohen SN, Curtiss III R, Datta N, Falkow S (1976) Uniform nomenclature for bacterial plasmids: a proposal. Bacteriol Rev 40:168–189Google Scholar
  35. Novick RP, Edelman I, Schwesinger MD, Gruss AD, Swanson EC, Pattee PA (1979) Genetic translocation in Staphylococcus aureus. Proc Natl Acad Sci USA 76:400–404Google Scholar
  36. Ounissi H, Courvalin P (1982) Heterogeneity of macrolide-lincosamide-streptogramin B-type antibiotic resistance determinants. In: Schlessinger D (ed) Microbiology-1982. American Society for Microbiology, Washington DC, pp 167–169Google Scholar
  37. Pakula R, Hulanicka E, Walczak W (1958) Transformation reactions between streptococci, pneumonocci, and staphylococci. Bull Acad Pol Sci 6:325–328Google Scholar
  38. Pérez-Diaz JC, Vicente MF, Baquero F (1982) Plasmids in Listeria. Plasmid 8:112–118Google Scholar
  39. Portnoy DA, Moseley SL, Flakow S (1981) Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis. Infect Immun 31:775–782Google Scholar
  40. Sanger F, Coulson AR, Hong GF, Hill DF, Petersen GB (1982) Nucleotide sequence of bacteriophage lambda DNA. J Mol Biol 162:729–773Google Scholar
  41. Shoemaker NB, Smith MD, Guild WR (1979) Organization and transfer of heterologous chloramphenicol and tetracycline resistance genes in Pneumococcus. J Bacteriol 139:432–441Google Scholar
  42. Shoemaker NB, Smith MD, Guild WR (1980) DNase-resistant transfer of chromosomal cat and tet insertions by filter mating in Pneumococcus. Plasmid 3:80–87Google Scholar
  43. Shinnick TM, Lund E, Smithies O, Blattner FR (1975) Hybridization of labeled RNA to DNA in agarose gels. Nucleic Acids Res 2:1911–1929Google Scholar
  44. Smith MD, Shoemaker NB, Burdett V, Guild WR (1980) Transfer of plasmids by conjugation in Streptococcus pneumoniae. Plasmid 3:70–79Google Scholar
  45. Southern E (1975) Detection of specific sequence among DNA fagments separated by gel electrophoresis. J Mol Biol 98:503–517Google Scholar
  46. Terzaghi BE, Sandine WE (1975) Improved medium for lactic streptococci and their bacteriophages. Appl Microbiol 29:807–813Google Scholar
  47. Trieu-Cuot P, Gerbaud G, Lambert T, Courvalin P (1985) In vivo transfer of genetic information between Gram-positive and Gram-negative bacteria. EMBO J 4:3583–3587Google Scholar
  48. Véron M, Chatelain R (1973) Taxonomic study of the genus Campylobacter Sebald and Véron and designation of the neotype strain for the type species Campylobacter fetus (Smith and Taylor) Sebald and Véron. Int J Syst Bact 23:122–134Google Scholar
  49. Yagi Y, Clewell DB (1980) Recombination-deficient mutant of Streptococcus faecalis. J Bacteriol 143:966–970Google Scholar

Copyright information

© springer-Verlag 1986

Authors and Affiliations

  • Patrice Courvalin
    • 1
  • Cécile Carlier
    • 1
  1. 1.Unité des Agents AntibactériensCNRS U.A. 271, Institut PasteurParis Cedex 15France

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