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. 1992 May;36(5):1005–1012. doi: 10.1128/aac.36.5.1005

A Bacteroides tetracycline resistance gene represents a new class of ribosome protection tetracycline resistance.

M P Nikolich 1, N B Shoemaker 1, A A Salyers 1
PMCID: PMC188826  PMID: 1339256

Abstract

The ribosome protection type of tetracycline resistance (Tcr) has been found in a variety of bacterial species, but the only two classes described previously, Tet(M) and Tet(O), shared a high degree of amino acid sequence identity (greater than 75%). Thus, it appeared that this type of resistance emerged recently in evolution and spread among different species of bacteria by horizontal transmission. We obtained the DNA sequence of a Tcr gene from Bacteroides, a genus of gram-negative, obligately anaerobic bacteria that is phylogenetically distant from the diverse species in which tet(M) and tet(O) have been found. The Bacteroides Tcr gene defines a new class of ribosome protection resistance genes, Tet(Q), and has a deduced amino acid sequence that was only 40% identical to Tet(M) or Tet(O). Like tet(M) and tet(O), tet(Q) appears to have spread by horizontal transmission, but only within the Bacteroides group.

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Selected References

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  1. Burdett V., Inamine J., Rajagopalan S. Heterogeneity of tetracycline resistance determinants in Streptococcus. J Bacteriol. 1982 Mar;149(3):995–1004. doi: 10.1128/jb.149.3.995-1004.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burdett V. Purification and characterization of Tet(M), a protein that renders ribosomes resistant to tetracycline. J Biol Chem. 1991 Feb 15;266(5):2872–2877. [PubMed] [Google Scholar]
  3. Burdett V. Streptococcal tetracycline resistance mediated at the level of protein synthesis. J Bacteriol. 1986 Feb;165(2):564–569. doi: 10.1128/jb.165.2.564-569.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. DeVries J. K., Zubay G. DNA-directed peptide synthesis. II. The synthesis of the alpha-fragment of the enzyme beta-galactosidase. Proc Natl Acad Sci U S A. 1967 Apr;57(4):1010–1012. doi: 10.1073/pnas.57.4.1010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Doyle D., McDowall K. J., Butler M. J., Hunter I. S. Characterization of an oxytetracycline-resistance gene, otrA, of Streptomyces rimosus. Mol Microbiol. 1991 Dec;5(12):2923–2933. doi: 10.1111/j.1365-2958.1991.tb01852.x. [DOI] [PubMed] [Google Scholar]
  7. Gawron-Burke C., Clewell D. B. Regeneration of insertionally inactivated streptococcal DNA fragments after excision of transposon Tn916 in Escherichia coli: strategy for targeting and cloning of genes from gram-positive bacteria. J Bacteriol. 1984 Jul;159(1):214–221. doi: 10.1128/jb.159.1.214-221.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Guiney D. G., Bouic K. Detection of conjugal transfer systems in oral, black-pigmented Bacteroides spp. J Bacteriol. 1990 Jan;172(1):495–497. doi: 10.1128/jb.172.1.495-497.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Guiney D. G., Hasegawa P., Davis C. E. Plasmid transfer from Escherichia coli to Bacteroides fragilis: differential expression of antibiotic resistance phenotypes. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7203–7206. doi: 10.1073/pnas.81.22.7203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Halliday K. R. Regional homology in GTP-binding proto-oncogene products and elongation factors. J Cyclic Nucleotide Protein Phosphor Res. 1983;9(6):435–448. [PubMed] [Google Scholar]
  11. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983 Jun 5;166(4):557–580. doi: 10.1016/s0022-2836(83)80284-8. [DOI] [PubMed] [Google Scholar]
  12. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  13. Jurnak F. Structure of the GDP domain of EF-Tu and location of the amino acids homologous to ras oncogene proteins. Science. 1985 Oct 4;230(4721):32–36. doi: 10.1126/science.3898365. [DOI] [PubMed] [Google Scholar]
  14. Knapp J. S., Johnson S. R., Zenilman J. M., Roberts M. C., Morse S. A. High-level tetracycline resistance resulting from TetM in strains of Neisseria spp., Kingella denitrificans, and Eikenella corrodens. Antimicrob Agents Chemother. 1988 May;32(5):765–767. doi: 10.1128/aac.32.5.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. LeBlanc D. J., Lee L. N., Titmas B. M., Smith C. J., Tenover F. C. Nucleotide sequence analysis of tetracycline resistance gene tetO from Streptococcus mutans DL5. J Bacteriol. 1988 Aug;170(8):3618–3626. doi: 10.1128/jb.170.8.3618-3626.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lederberg E. M., Cohen S. N. Transformation of Salmonella typhimurium by plasmid deoxyribonucleic acid. J Bacteriol. 1974 Sep;119(3):1072–1074. doi: 10.1128/jb.119.3.1072-1074.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Manavathu E. K., Hiratsuka K., Taylor D. E. Nucleotide sequence analysis and expression of a tetracycline-resistance gene from Campylobacter jejuni. Gene. 1988;62(1):17–26. doi: 10.1016/0378-1119(88)90576-8. [DOI] [PubMed] [Google Scholar]
  18. Martin P., Trieu-Cuot P., Courvalin P. Nucleotide sequence of the tetM tetracycline resistance determinant of the streptococcal conjugative shuttle transposon Tn1545. Nucleic Acids Res. 1986 Sep 11;14(17):7047–7058. doi: 10.1093/nar/14.17.7047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Needleman S. B., Wunsch C. D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol. 1970 Mar;48(3):443–453. doi: 10.1016/0022-2836(70)90057-4. [DOI] [PubMed] [Google Scholar]
  20. Nesin M., Svec P., Lupski J. R., Godson G. N., Kreiswirth B., Kornblum J., Projan S. J. Cloning and nucleotide sequence of a chromosomally encoded tetracycline resistance determinant, tetA(M), from a pathogenic, methicillin-resistant strain of Staphylococcus aureus. Antimicrob Agents Chemother. 1990 Nov;34(11):2273–2276. doi: 10.1128/aac.34.11.2273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Odelson D. A., Rasmussen J. L., Smith C. J., Macrina F. L. Extrachromosomal systems and gene transmission in anaerobic bacteria. Plasmid. 1987 Mar;17(2):87–109. doi: 10.1016/0147-619x(87)90016-3. [DOI] [PubMed] [Google Scholar]
  22. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  24. Roberts M. C. Characterization of the Tet M determinants in urogenital and respiratory bacteria. Antimicrob Agents Chemother. 1990 Mar;34(3):476–478. doi: 10.1128/aac.34.3.476. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Roberts M. C., Hillier S. L. Genetic basis of tetracycline resistance in urogenital bacteria. Antimicrob Agents Chemother. 1990 Feb;34(2):261–264. doi: 10.1128/aac.34.2.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Roberts M. C., Koutsky L. A., Holmes K. K., LeBlanc D. J., Kenny G. E. Tetracycline-resistant Mycoplasma hominis strains contain streptococcal tetM sequences. Antimicrob Agents Chemother. 1985 Jul;28(1):141–143. doi: 10.1128/aac.28.1.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Roberts M. C., Moncla B. J. Tetracycline resistance and TetM in oral anaerobic bacteria and Neisseria perflava-N. sicca. Antimicrob Agents Chemother. 1988 Aug;32(8):1271–1273. doi: 10.1128/aac.32.8.1271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. SAITO H., MIURA K. I. PREPARATION OF TRANSFORMING DEOXYRIBONUCLEIC ACID BY PHENOL TREATMENT. Biochim Biophys Acta. 1963 Aug 20;72:619–629. [PubMed] [Google Scholar]
  29. Salyers A. A., Shoemaker N. B., Guthrie E. P. Recent advances in Bacteroides genetics. Crit Rev Microbiol. 1987;14(1):49–71. doi: 10.3109/10408418709104435. [DOI] [PubMed] [Google Scholar]
  30. Salyers A. A., Speer B. S., Shoemaker N. B. New perspectives in tetracycline resistance. Mol Microbiol. 1990 Jan;4(1):151–156. doi: 10.1111/j.1365-2958.1990.tb02025.x. [DOI] [PubMed] [Google Scholar]
  31. Sancar A., Hack A. M., Rupp W. D. Simple method for identification of plasmid-coded proteins. J Bacteriol. 1979 Jan;137(1):692–693. doi: 10.1128/jb.137.1.692-693.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sanchez-Pescador R., Brown J. T., Roberts M., Urdea M. S. The nucleotide sequence of the tetracycline resistance determinant tetM from Ureaplasma urealyticum. Nucleic Acids Res. 1988 Feb 11;16(3):1216–1217. doi: 10.1093/nar/16.3.1216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Shoemaker N. B., Guthrie E. P., Salyers A. A., Gardner J. F. Evidence that the clindamycin-erythromycin resistance gene of Bacteroides plasmid pBF4 is on a transposable element. J Bacteriol. 1985 May;162(2):626–632. doi: 10.1128/jb.162.2.626-632.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shoemaker N. B., Salyers A. A. A cryptic 65-kilobase-pair transposonlike element isolated from Bacteroides uniformis has homology with Bacteroides conjugal tetracycline resistance elements. J Bacteriol. 1990 Apr;172(4):1694–1702. doi: 10.1128/jb.172.4.1694-1702.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Smith C. J. Nucleotide sequence analysis of Tn4551: use of ermFS operon fusions to detect promoter activity in Bacteroides fragilis. J Bacteriol. 1987 Oct;169(10):4589–4596. doi: 10.1128/jb.169.10.4589-4596.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Speer B. S., Salyers A. A. Characterization of a novel tetracycline resistance that functions only in aerobically grown Escherichia coli. J Bacteriol. 1988 Apr;170(4):1423–1429. doi: 10.1128/jb.170.4.1423-1429.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Stevens A. M., Shoemaker N. B., Salyers A. A. The region of a Bacteroides conjugal chromosomal tetracycline resistance element which is responsible for production of plasmidlike forms from unlinked chromosomal DNA might also be involved in transfer of the element. J Bacteriol. 1990 Aug;172(8):4271–4279. doi: 10.1128/jb.172.8.4271-4279.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Tally F. P., Cuchural G. J., Jr, Jacobus N. V., Gorbach S. L., Aldridge K., Cleary T., Finegold S. M., Hill G., Iannini P., O'Keefe J. P. Nationwide study of the susceptibility of the Bacteroides fragilis group in the United States. Antimicrob Agents Chemother. 1985 Nov;28(5):675–677. doi: 10.1128/aac.28.5.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Taylor D. E. Plasmid-mediated tetracycline resistance in Campylobacter jejuni: expression in Escherichia coli and identification of homology with streptococcal class M determinant. J Bacteriol. 1986 Mar;165(3):1037–1039. doi: 10.1128/jb.165.3.1037-1039.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Tenover F. C., LeBlanc D. J., Elvrum P. Cloning and expression of a tetracycline resistance determinant from Campylobacter jejuni in Escherichia coli. Antimicrob Agents Chemother. 1987 Sep;31(9):1301–1306. doi: 10.1128/aac.31.9.1301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Thompson J. S., Malamy M. H. Sequencing the gene for an imipenem-cefoxitin-hydrolyzing enzyme (CfiA) from Bacteroides fragilis TAL2480 reveals strong similarity between CfiA and Bacillus cereus beta-lactamase II. J Bacteriol. 1990 May;172(5):2584–2593. doi: 10.1128/jb.172.5.2584-2593.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Valentine P. J., Shoemaker N. B., Salyers A. A. Mobilization of Bacteroides plasmids by Bacteroides conjugal elements. J Bacteriol. 1988 Mar;170(3):1319–1324. doi: 10.1128/jb.170.3.1319-1324.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zilhao R., Papadopoulou B., Courvalin P. Occurrence of the Campylobacter resistance gene tetO in Enterococcus and Streptococcus spp. Antimicrob Agents Chemother. 1988 Dec;32(12):1793–1796. doi: 10.1128/aac.32.12.1793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. de Barbeyrac B., Dutilh B., Quentin C., Renaudin H., Bébéar C. Susceptibility of Bacteroides ureolyticus to antimicrobial agents and identification of a tetracycline resistance determinant related to tetM. J Antimicrob Chemother. 1991 Jun;27(6):721–731. doi: 10.1093/jac/27.6.721. [DOI] [PubMed] [Google Scholar]
  45. de Veaux L. C., Clevenson D. S., Bradbeer C., Kadner R. J. Identification of the btuCED polypeptides and evidence for their role in vitamin B12 transport in Escherichia coli. J Bacteriol. 1986 Sep;167(3):920–927. doi: 10.1128/jb.167.3.920-927.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]

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