Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1988 Apr;170(4):1739–1745. doi: 10.1128/jb.170.4.1739-1745.1988

Evidence for natural gene transfer from gram-positive cocci to Escherichia coli.

A Brisson-Noël 1, M Arthur 1, P Courvalin 1
PMCID: PMC211025  PMID: 2832378

Abstract

High-level resistance to macrolide-lincosamide-streptogramin type B (MLS) antibiotics in Escherichia coli BM2570 is due to the presence on the conjugative plasmid pIP1527 of the MLS resistance determinant ermBC, which is almost identical to the erm genes previously described in plasmid pAM77 from Streptococcus sanguis (ermAM) and in transposon Tn917 from Enterococcus faecalis (ermB). This gene and its regulatory region are located downstream from the insertion sequence IS1. The 23S rRNA methylase encoded by pIP1527 differs by three and six amino acids from those encoded by Tn917 and pAM77, respectively. Unlike the streptococcal elements which confer the inducible MLS phenotype, the ermBC gene is expressed constitutively in E. coli and Bacillus subtilis, due to several mutations in the regulatory region. Transcription of the ermBC gene starts from three different sites following three overlapping promoters which function in both E. coli and B. subtilis. Promoters P2 and P3 are located within the region homologous to pAM77 and Tn917, and P1 is a hybrid promoter constituted by -35 and -10 sequences located at the end of IS15 and in the streptococcal region, respectively. These results constitute evidence for the recent in vivo transfer from Streptococcus spp. to E. coli. This transfer could have been mediated by transposons such as Tn917 or Tn1545 from Streptococcus pneumoniae, which also bears an MLS determinant that is homologous to ermB. We speculate that the insertion sequences IS15 and IS1 could have played a role in the expression and dissemination of ermBC, which has been found in numerous strains of enterobacteria.

Full text

PDF
1745

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allmansberger R., Bräu B., Piepersberg W. 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. 1985;198(3):514–520. doi: 10.1007/BF00332949. [DOI] [PubMed] [Google Scholar]
  2. Andremont A., Raibaud P., Tancrède C. Effect of erythromycin on microbial antagonisms: a study in gnotobiotic mice associated with a human fecal flora. J Infect Dis. 1983 Sep;148(3):579–587. doi: 10.1093/infdis/148.3.579. [DOI] [PubMed] [Google Scholar]
  3. Andremont A., Sancho-Garnier H., Tancrede C. Epidemiology of intestinal colonization by members of the family Enterobacteriaceae highly resistant to erythromycin in a hematology-oncology unit. Antimicrob Agents Chemother. 1986 Jun;29(6):1104–1107. doi: 10.1128/aac.29.6.1104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Arthur M., Andremont A., Courvalin P. Distribution of erythromycin esterase and rRNA methylase genes in members of the family Enterobacteriaceae highly resistant to erythromycin. Antimicrob Agents Chemother. 1987 Mar;31(3):404–409. doi: 10.1128/aac.31.3.404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Arthur M., Autissier D., Courvalin P. Analysis of the nucleotide sequence of the ereB gene encoding the erythromycin esterase type II. Nucleic Acids Res. 1986 Jun 25;14(12):4987–4999. doi: 10.1093/nar/14.12.4987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Arthur M., Brisson-Noël A., Courvalin P. Origin and evolution of genes specifying resistance to macrolide, lincosamide and streptogramin antibiotics: data and hypotheses. J Antimicrob Chemother. 1987 Dec;20(6):783–802. doi: 10.1093/jac/20.6.783. [DOI] [PubMed] [Google Scholar]
  7. Arthur M., Courvalin P. Contribution of two different mechanisms to erythromycin resistance in Escherichia coli. Antimicrob Agents Chemother. 1986 Nov;30(5):694–700. doi: 10.1128/aac.30.5.694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bräu B., Pilz U., Piepersberg W. 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. 1984;193(1):179–187. doi: 10.1007/BF00327434. [DOI] [PubMed] [Google Scholar]
  9. Courvalin P., Carlier C. Tn1545: a conjugative shuttle transposon. Mol Gen Genet. 1987 Feb;206(2):259–264. doi: 10.1007/BF00333582. [DOI] [PubMed] [Google Scholar]
  10. Datta N., Hedges R. W., Becker D., Davies J. Plasmid-determined fusidic acid resistance in the Enterobacteriaceae. J Gen Microbiol. 1974 Jul;83(0):191–196. doi: 10.1099/00221287-83-1-191. [DOI] [PubMed] [Google Scholar]
  11. Denoya C. D., Dubnau D. Site and substrate specificity of the ermC 23S rRNA methyltransferase. J Bacteriol. 1987 Aug;169(8):3857–3860. doi: 10.1128/jb.169.8.3857-3860.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Débarbouillé M., Raibaud O. Expression of the Escherichia coli malPQ operon remains unaffected after drastic alteration of its promoter. J Bacteriol. 1983 Mar;153(3):1221–1227. doi: 10.1128/jb.153.3.1221-1227.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ehrlich S. D. DNA cloning in Bacillus subtilis. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1433–1436. doi: 10.1073/pnas.75.3.1433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gryczan T. J., Grandi G., Hahn J., Grandi R., Dubnau D. Conformational alteration of mRNA structure and the posttranscriptional regulation of erythromycin-induced drug resistance. Nucleic Acids Res. 1980 Dec 20;8(24):6081–6097. doi: 10.1093/nar/8.24.6081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gryczan T., Israeli-Reches M., Del Bue M., Dubnau D. DNA sequence and regulation of ermD, a macrolide-lincosamide-streptogramin B resistance element from Bacillus licheniformis. Mol Gen Genet. 1984;194(3):349–356. doi: 10.1007/BF00425543. [DOI] [PubMed] [Google Scholar]
  16. Hardy K., Haefeli C. Expression in Escherichia coli of a staphylococcal gene for resistance to macrolide, lincosamide, and streptogramin type B antibiotics. J Bacteriol. 1982 Oct;152(1):524–526. doi: 10.1128/jb.152.1.524-526.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Horinouchi S., Byeon W. H., Weisblum B. A complex attenuator regulates inducible resistance to macrolides, lincosamides, and streptogramin type B antibiotics in Streptococcus sanguis. J Bacteriol. 1983 Jun;154(3):1252–1262. doi: 10.1128/jb.154.3.1252-1262.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Horinouchi S., Weisblum B. Nucleotide sequence and functional map of pC194, a plasmid that specifies inducible chloramphenicol resistance. J Bacteriol. 1982 May;150(2):815–825. doi: 10.1128/jb.150.2.815-825.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Horinouchi S., Weisblum B. Nucleotide sequence and functional map of pE194, a plasmid that specifies inducible resistance to macrolide, lincosamide, and streptogramin type B antibodies. J Bacteriol. 1982 May;150(2):804–814. doi: 10.1128/jb.150.2.804-814.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Horinouchi S., Weisblum B. The control region for erythromycin resistance: free energy changes related to induction and mutation to constitutive expression. Mol Gen Genet. 1981;182(2):341–348. doi: 10.1007/BF00269681. [DOI] [PubMed] [Google Scholar]
  21. Kleckner N. Transposable elements in prokaryotes. Annu Rev Genet. 1981;15:341–404. doi: 10.1146/annurev.ge.15.120181.002013. [DOI] [PubMed] [Google Scholar]
  22. Kuramitsu H. K., Casadaban M. J. Transposition of the gram-positive transposon Tn917 in Escherichia coli. J Bacteriol. 1986 Aug;167(2):711–712. doi: 10.1128/jb.167.2.711-712.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Malke H., Holm S. E. Expression of streptococcal plasmid-determined resistance to erythromycin and lincomycin in Escherichia coli. Mol Gen Genet. 1981;184(2):283–285. doi: 10.1007/BF00272918. [DOI] [PubMed] [Google Scholar]
  24. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  25. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  26. Monod M., Mohan S., Dubnau D. Cloning and analysis of ermG, a new macrolide-lincosamide-streptogramin B resistance element from Bacillus sphaericus. J Bacteriol. 1987 Jan;169(1):340–350. doi: 10.1128/jb.169.1.340-350.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Morse S. A., Johnson S. R., Biddle J. W., Roberts M. C. High-level tetracycline resistance in Neisseria gonorrhoeae is result of acquisition of streptococcal tetM determinant. Antimicrob Agents Chemother. 1986 Nov;30(5):664–670. doi: 10.1128/aac.30.5.664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Murphy E. Nucleotide sequence of ermA, a macrolide-lincosamide-streptogramin B determinant in Staphylococcus aureus. J Bacteriol. 1985 May;162(2):633–640. doi: 10.1128/jb.162.2.633-640.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ohtsubo H., Ohtsubo E. Nucleotide sequence of an insertion element, IS1. Proc Natl Acad Sci U S A. 1978 Feb;75(2):615–619. doi: 10.1073/pnas.75.2.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rasmussen J. L., Odelson D. A., Macrina F. L. Complete nucleotide sequence and transcription of ermF, a macrolide-lincosamide-streptogramin B resistance determinant from Bacteroides fragilis. J Bacteriol. 1986 Nov;168(2):523–533. doi: 10.1128/jb.168.2.523-533.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Roberts A. N., Hudson G. S., Brenner S. An erythromycin-resistance gene from an erythromycin-producing strain of Arthrobacter sp. Gene. 1985;35(3):259–270. doi: 10.1016/0378-1119(85)90004-6. [DOI] [PubMed] [Google Scholar]
  32. Rosenberg M., Court D. Regulatory sequences involved in the promotion and termination of RNA transcription. Annu Rev Genet. 1979;13:319–353. doi: 10.1146/annurev.ge.13.120179.001535. [DOI] [PubMed] [Google Scholar]
  33. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shaw J. H., Clewell D. B. Complete nucleotide sequence of macrolide-lincosamide-streptogramin B-resistance transposon Tn917 in Streptococcus faecalis. J Bacteriol. 1985 Nov;164(2):782–796. doi: 10.1128/jb.164.2.782-796.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sollner-Webb B., Reeder R. H. The nucleotide sequence of the initiation and termination sites for ribosomal RNA transcription in X. laevis. Cell. 1979 Oct;18(2):485–499. doi: 10.1016/0092-8674(79)90066-7. [DOI] [PubMed] [Google Scholar]
  36. Spizizen J. TRANSFORMATION OF BIOCHEMICALLY DEFICIENT STRAINS OF BACILLUS SUBTILIS BY DEOXYRIBONUCLEATE. Proc Natl Acad Sci U S A. 1958 Oct 15;44(10):1072–1078. doi: 10.1073/pnas.44.10.1072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Staden R. A new computer method for the storage and manipulation of DNA gel reading data. Nucleic Acids Res. 1980 Aug 25;8(16):3673–3694. doi: 10.1093/nar/8.16.3673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Thakker-Varia S., Jenssen W. D., Moon-McDermott L., Weinstein M. P., Dubin D. T. Molecular epidemiology of macrolides-lincosamides-streptogramin B resistance in Staphylococcus aureus and coagulase-negative staphylococci. Antimicrob Agents Chemother. 1987 May;31(5):735–743. doi: 10.1128/aac.31.5.735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Thakker-Varia S., Ranzini A. C., Dubin D. T. Ribosomal RNA methylation in Staphylococcus aureus and Escherichia coli: effect of the "MLS" (erythromycin resistance) methylase. Plasmid. 1985 Sep;14(2):152–161. doi: 10.1016/0147-619x(85)90075-7. [DOI] [PubMed] [Google Scholar]
  40. Tinoco I., Jr, Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973 Nov 14;246(150):40–41. doi: 10.1038/newbio246040a0. [DOI] [PubMed] [Google Scholar]
  41. Trieu-Cuot P., Courvalin P. Nucleotide sequence of the transposable element IS15. Gene. 1984 Oct;30(1-3):113–120. doi: 10.1016/0378-1119(84)90111-2. [DOI] [PubMed] [Google Scholar]
  42. Trieu-Cuot P., Gerbaud G., Lambert T., Courvalin P. In vivo transfer of genetic information between gram-positive and gram-negative bacteria. EMBO J. 1985 Dec 16;4(13A):3583–3587. doi: 10.1002/j.1460-2075.1985.tb04120.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Uchiyama H., Weisblum B. N-Methyl transferase of Streptomyces erythraeus that confers resistance to the macrolide-lincosamide-streptogramin B antibiotics: amino acid sequence and its homology to cognate R-factor enzymes from pathogenic bacilli and cocci. Gene. 1985;38(1-3):103–110. doi: 10.1016/0378-1119(85)90208-2. [DOI] [PubMed] [Google Scholar]
  44. Weisblum B., Graham M. Y., Gryczan T., Dubnau D. Plasmid copy number control: isolation and characterization of high-copy-number mutants of plasmid pE194. J Bacteriol. 1979 Jan;137(1):635–643. doi: 10.1128/jb.137.1.635-643.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Weisblum B., Holder S. B., Halling S. M. Deoxyribonucleic acid sequence common to staphylococcal and streptococcal plasmids which specify erythromycin resistance. J Bacteriol. 1979 Jun;138(3):990–998. doi: 10.1128/jb.138.3.990-998.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wilbur W. J., Lipman D. J. Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci U S A. 1983 Feb;80(3):726–730. doi: 10.1073/pnas.80.3.726. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES