Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1996 Apr;178(7):1914–1918. doi: 10.1128/jb.178.7.1914-1918.1996

A recent fixation of cfiA genes in a monophyletic cluster of Bacteroides fragilis is correlated with the presence of multiple insertion elements.

R Ruimy 1, I Podglajen 1, J Breuil 1, R Christen 1, E Collatz 1
PMCID: PMC177886  PMID: 8606165

Abstract

Small-subunit ribosomal DNA sequences of 16 strains of Bacteroides fragilis were determined and compared with previously published sequences. Three phylogenetic methods (the neighbor-joining, maximum-likelihood, and maximum-parsimony methods) as well as a bootstrap analysis were used to assess the robustness of each topology. All phylogenetic analyses demonstrated that the B. fragilis strains were clearly divided into two robust monophyletic units which corresponded to the cfiA-negative and cfiA-positive groups. Strains of two previously identified DNA homology groups separated similarly into the two monophyletic units. According to the intensity of the hybridization signal with a cfiA probe, the cfiA-positive cluster could be further divided into two groups. This difference might reflect the existence of two, probably closely related cfiA-type genes. In the strongly hybridizing cfiA-positive strains, the gene is capable of conferring high-level resistance to the carbapenems and to most beta-lactamase inhibitors as well, while in the weakly hybridizing cfiA-positive strains, only the latter type of resistance is known to occur. The presence of the cfiA-type genes within a monophyletic cluster of B. fragilis that apparently represents only a minority of the species B. fragilis is suggestive of a recent acquisition. The fact that this cluster is also the predominant pool of all known B. fragilis insertion elements, which have been found to play an important role in the expression of carbapenem resistance, raises the possibility that both genetic determinants, i.e., the resistance gene(s) and insertion elements, may have coevolved.

Full Text

The Full Text of this article is available as a PDF (251.6 KB).

Selected References

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

  1. Ambler R. P. The structure of beta-lactamases. Philos Trans R Soc Lond B Biol Sci. 1980 May 16;289(1036):321–331. doi: 10.1098/rstb.1980.0049. [DOI] [PubMed] [Google Scholar]
  2. Appelbaum P. C., Jacobs M. R., Spangler S. K., Yamabe S. Comparative activity of beta-lactamase inhibitors YTR 830, clavulanate, and sulbactam combined with beta-lactams against beta-lactamase-producing anaerobes. Antimicrob Agents Chemother. 1986 Nov;30(5):789–791. doi: 10.1128/aac.30.5.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Appleman M. D., Heseltine P. N., Cherubin C. E. Epidemiology, antimicrobial susceptibility, pathogenicity, and significance of Bacteroides fragilis group organisms isolated at Los Angeles County-University of Southern California Medical Center. Rev Infect Dis. 1991 Jan-Feb;13(1):12–18. doi: 10.1093/clinids/13.1.12. [DOI] [PubMed] [Google Scholar]
  4. Cornick N. A., Cuchural G. J., Jr, Snydman D. R., Jacobus N. V., Iannini P., Hill G., Cleary T., O'Keefe J. P., Pierson C., Finegold S. M. The antimicrobial susceptibility patterns of the Bacteroides fragilis group in the United States, 1987. J Antimicrob Chemother. 1990 Jun;25(6):1011–1019. doi: 10.1093/jac/25.6.1011. [DOI] [PubMed] [Google Scholar]
  5. Cuchural G. J., Jr, Malamy M. H., Tally F. P. Beta-lactamase-mediated imipenem resistance in Bacteroides fragilis. Antimicrob Agents Chemother. 1986 Nov;30(5):645–648. doi: 10.1128/aac.30.5.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Eley A., Greenwood D. Beta-lactamases of type culture strains of the Bacteroides fragilis group and of strains that hydrolyse cefoxitin, latamoxef and imipenem. J Med Microbiol. 1986 Feb;21(1):49–57. doi: 10.1099/00222615-21-1-49. [DOI] [PubMed] [Google Scholar]
  7. Gherna R., Woese C. R. A partial phylogenetic analysis of the "flavobacter-bacteroides" phylum: basis for taxonomic restructuring. Syst Appl Microbiol. 1992 Dec;15(4):513–521. doi: 10.1016/S0723-2020(11)80110-4. [DOI] [PubMed] [Google Scholar]
  8. Hedberg M., Edlund C., Lindqvist L., Rylander M., Nord C. E. Purification and characterization of an imipenem hydrolysing metallo-beta-lactamase from Bacteroides fragilis. J Antimicrob Chemother. 1992 Feb;29(2):105–113. doi: 10.1093/jac/29.2.105. [DOI] [PubMed] [Google Scholar]
  9. Jacobs M. R., Spangler S. K., Appelbaum P. C. beta-Lactamase production and susceptibility of US and European anaerobic gram-negative bacilli to beta-lactams and other agents. Eur J Clin Microbiol Infect Dis. 1992 Nov;11(11):1081–1093. doi: 10.1007/BF01967803. [DOI] [PubMed] [Google Scholar]
  10. Olsen G. J., Woese C. R. Ribosomal RNA: a key to phylogeny. FASEB J. 1993 Jan;7(1):113–123. doi: 10.1096/fasebj.7.1.8422957. [DOI] [PubMed] [Google Scholar]
  11. Parker A. C., Smith C. J. Genetic and biochemical analysis of a novel Ambler class A beta-lactamase responsible for cefoxitin resistance in Bacteroides species. Antimicrob Agents Chemother. 1993 May;37(5):1028–1036. doi: 10.1128/aac.37.5.1028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Paster B. J., Dewhirst F. E., Olsen I., Fraser G. J. Phylogeny of Bacteroides, Prevotella, and Porphyromonas spp. and related bacteria. J Bacteriol. 1994 Feb;176(3):725–732. doi: 10.1128/jb.176.3.725-732.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Patey O., Varon E., Prazuck T., Podglajen I., Dublanchet A., Dubreuil L., Breuil J. Multicentre survey in France of the antimicrobial susceptibilities of 416 blood culture isolates of the Bacteroides fragilis group. J Antimicrob Chemother. 1994 May;33(5):1029–1034. doi: 10.1093/jac/33.5.1029. [DOI] [PubMed] [Google Scholar]
  14. Podglajen I., Breuil J., Bordon F., Gutmann L., Collatz E. A silent carbapenemase gene in strains of Bacteroides fragilis can be expressed after a one-step mutation. FEMS Microbiol Lett. 1992 Feb 1;70(1):21–29. doi: 10.1016/0378-1097(92)90557-5. [DOI] [PubMed] [Google Scholar]
  15. Podglajen I., Breuil J., Casin I., Collatz E. Genotypic identification of two groups within the species Bacteroides fragilis by ribotyping and by analysis of PCR-generated fragment patterns and insertion sequence content. J Bacteriol. 1995 Sep;177(18):5270–5275. doi: 10.1128/jb.177.18.5270-5275.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Podglajen I., Breuil J., Collatz E. Insertion of a novel DNA sequence, 1S1186, upstream of the silent carbapenemase gene cfiA, promotes expression of carbapenem resistance in clinical isolates of Bacteroides fragilis. Mol Microbiol. 1994 Apr;12(1):105–114. doi: 10.1111/j.1365-2958.1994.tb00999.x. [DOI] [PubMed] [Google Scholar]
  17. Privitera G., Dublanchet A., Sebald M. Transfer of multiple antibiotic resistance between subspecies of Bacteroides fragilis. J Infect Dis. 1979 Jan;139(1):97–101. doi: 10.1093/infdis/139.1.97. [DOI] [PubMed] [Google Scholar]
  18. Rasmussen B. A., Gluzman Y., Tally F. P. Cloning and sequencing of the class B beta-lactamase gene (ccrA) from Bacteroides fragilis TAL3636. Antimicrob Agents Chemother. 1990 Aug;34(8):1590–1592. doi: 10.1128/aac.34.8.1590. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rasmussen B. A., Kovacs E. Identification and DNA sequence of a new Bacteroides fragilis insertion sequence-like element. Plasmid. 1991 Mar;25(2):141–144. doi: 10.1016/0147-619x(91)90027-t. [DOI] [PubMed] [Google Scholar]
  20. Rasmussen J. L., Odelson D. A., Macrina F. L. Complete nucleotide sequence of insertion element IS4351 from Bacteroides fragilis. J Bacteriol. 1987 Aug;169(8):3573–3580. doi: 10.1128/jb.169.8.3573-3580.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rogers M. B., Parker A. C., Smith C. J. Cloning and characterization of the endogenous cephalosporinase gene, cepA, from Bacteroides fragilis reveals a new subgroup of Ambler class A beta-lactamases. Antimicrob Agents Chemother. 1993 Nov;37(11):2391–2400. doi: 10.1128/aac.37.11.2391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ruimy R., Breittmayer V., Elbaze P., Lafay B., Boussemart O., Gauthier M., Christen R. Phylogenetic analysis and assessment of the genera Vibrio, Photobacterium, Aeromonas, and Plesiomonas deduced from small-subunit rRNA sequences. Int J Syst Bacteriol. 1994 Jul;44(3):416–426. doi: 10.1099/00207713-44-3-416. [DOI] [PubMed] [Google Scholar]
  23. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Weisburg W. G., Oyaizu Y., Oyaizu H., Woese C. R. Natural relationship between bacteroides and flavobacteria. J Bacteriol. 1985 Oct;164(1):230–236. doi: 10.1128/jb.164.1.230-236.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wüst J., Wilkins T. D. Effect of clavulanic Acid on anaerobic bacteria resistant to Beta-lactam antibiotics. Antimicrob Agents Chemother. 1978 Jan;13(1):130–133. doi: 10.1128/aac.13.1.130. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES