Skip to main content
Log in

Can beta-lactamase resistance genes in anaerobic Gram-negative gut bacteria transfer to gut aerobes?

  • Brief Communication
  • Published:
The Journal of Antibiotics Submit manuscript

Abstract

The study was conceived with the hypothesis that human aerobic gut flora could act as a reservoir of ß-lactamases and contribute to the emergence of ß-lactam resistance by transferring ß-lactamase genes to resident anaerobes. Thus, we studied the repertoire of ß-lactam resistance determinants (ß-lactamases associated with aerobes and anaerobes) in Gram-negative anaerobes. The phenotypic resistance against ß-lactams and the presence of aerobic and anaerobic ß-lactamases were tested in Gram-negative anaerobic isolates (n = 200) by agar dilution method and targeted PCR, respectively. In addition, whole-genome sequencing (WGS) was used to study the ß-lactam resistance determinants in 4/200 multi-drug resistant (MDR) strains. The resistance to ß-lactams was as follows: imipenem (0.5%), cefoxitin (26.5%), and piperacillin–tazobactam (27.5%). None of the isolates showed the presence of ß-lactamases found in aerobic microorganisms. The presence of anaerobic ß-lactamase genes viz. cfiA, cepA, cfxA, cfiAIS [the intact segment containing cfiA gene (350 bp) and upstream IS elements (1.6–1.7 kb)] was detected in 10%, 9.5%, 21.5%, and 0% isolates, respectively. The WGS data showed the presence of cfiA, cfiA4, cfxA, cfxA2, cfxA3, cfxA4, cfxA5 in MDR strains. The study showed a distinct dichotomy in repertoires of ß-lactamases between aerobes and anaerobes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Data availability

The bacterial genome data are submitted to the Figshare repository (https://doi.org/10.6084/m9.figshare.20267595).

References

  1. Smillie CS, Smith MB, Friedman J, Cordero OX, David LA, Alm EJ. Ecology drives a global network of gene exchange connecting the human microbiome. Nature. 2011;480:241–4.

    Article  CAS  PubMed  Google Scholar 

  2. Hedberg M, Nord CE. Beta-lactam resistance in anaerobic bacteria: a review. J Chemother. 1996;8:3–16.

    Article  CAS  PubMed  Google Scholar 

  3. Sood A, Ray P, Angrup A. Phenotypic and genotypic antimicrobial resistance in clinical anaerobic isolates from India. JAC Antimicrob Resist. 2021;3:1–9.

    Article  Google Scholar 

  4. Angrup A, Sood A, Ray P, Bala K. Clinical anaerobic infections in an Indian tertiary care hospital: a two-year retrospective study. Anaerobe. 2021;73:102482.

    Article  PubMed  Google Scholar 

  5. Sood A, Angrup A, Ray P, Bala K. Comparative evaluation of agar dilution and broth microdilution by commercial and in-house plates for Bacteroides fragilis group: an economical and expeditious approach for resource-limited settings. Anaerobe. 2021;71:102443.

    Article  CAS  PubMed  Google Scholar 

  6. Sood A, Ray P, Angrup A. Antimicrobial susceptibility testing of anaerobic bacteria: in routine and research. Anaerobe. 2022;75:102559.

    Article  CAS  PubMed  Google Scholar 

  7. Dallenne C, da Costa A, Decré D, Favier C, Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important β-lactamases in Enterobacteriaceae. J Antimicrob Chemother. 2010;65:490–5.

    Article  CAS  PubMed  Google Scholar 

  8. Aziz RK, et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics. 2008;9:75.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Alcock BP, et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res. 2020;48:D517–25.

    CAS  PubMed  Google Scholar 

  10. Bortolaia V, et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother. 2020;75:3491–500.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Guiney DG, Hasegawa P, Davis CE. Plasmid transfer from Escherichia coli to Bacteroides fragilis: differential expression of antibiotic resistance phenotypes. Proc Natl Acad Sci USA. 1984;81:7203–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. SJ G, et al. Genome streamlining in a cosmopolitan oceanic bacterium. Science. 2005;309:1242–5.

    Article  Google Scholar 

  13. Jain R, Rivera MC, Moore JE, Lake JA. Horizontal gene transfer accelerates genome innovation and evolution. Mol Biol Evol. 2003;20:1598–602.

    Article  CAS  PubMed  Google Scholar 

  14. Roux D, et al. Fitness cost of antibiotic susceptibility during bacterial infection. Sci Transl Med. 2015;7:297ra114.

  15. Nakano V, Nascimento e Silva AD, Merino VRC, Wexler HM, Avila-Campos MJ. Antimicrobial resistance and prevalence of resistance genes in intestinal Bacteroidales strains. Clinics. 2011;66:543–7.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Kato N, Yamazoe K, Han CG, Ohtsubo E. New insertion sequence elements in the upstream region of cfiA in imipenem-resistant Bacteroides fragilis strains. Antimicrob Agents Chemother. 2003;47:979–85.

    Article  CAS  Google Scholar 

  17. Veloo ACM, Baas WH, Haan FJ, Coco J, Rossen JW. Prevalence of antimicrobial resistance genes in Bacteroides spp. and Prevotella spp. Dutch clinical isolates. Clin Microbiol Infect. 2019;25:1156.e9–13.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We acknowledge the support provided by the Department of Medical Microbiology, PGIMER, Chandigarh.

Funding

This work was supported by the Indian Council of Medical Research extramural grant (AMR/ADHOC/181/2019-ECD-II).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Archana Angrup.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sood, A., Sharma, V., Ray, P. et al. Can beta-lactamase resistance genes in anaerobic Gram-negative gut bacteria transfer to gut aerobes?. J Antibiot 76, 355–359 (2023). https://doi.org/10.1038/s41429-023-00608-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41429-023-00608-z

  • Springer Japan KK

Navigation