Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Study on the mechanisms of the cross-resistance to TET, PIP, and GEN in Staphylococcus aureus mediated by the Rhizoma Coptidis extracts

The Journal of Antibiotics volume 74, pages 330–336 (2021)Cite this article

Subjects

Abstract

The purpose of this study was focused on the mechanisms of the cross-resistance to tetracycline (TET), piperacillin Sodium (PIP), and gentamicin (GEN) in Staphylococcus aureus (SA) mediated by Rhizoma Coptidis extracts (RCE). The selected strains were exposed continuously to RCE at the sublethal concentrations for 12 days, respectively. The susceptibility change of the drug-exposed strains was determined by analysis of the minimum inhibitory concentration. The 16S rDNA sequencing method was used to identify the RCE-exposed strain. Then the expression of resistant genes in the selected isolates was analyzed by transcriptome sequencing. The results indicated that RCE could trigger the preferential cross-resistance to TET, PIP, and GEN in SA. The correlative resistant genes to the three kinds of antibiotics were upregulated in the RCE-exposed strain, and the mRNA levels of the resistant genes determined by RT-qPCR were consistent with those from the transcriptome analysis. It was suggested from these results that the antibacterial Traditional Chinese Medicines might be a significant factor of causing the bacterial antibiotic-resistance.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1

Similar content being viewed by others

Data availability

The tables data used to support the findings of this study are included within the article.

References

  1. Tishler PV. Production of penicillin. N Engl J Med. 2005;352:97.

    Article  CAS  PubMed  Google Scholar 

  2. Russell AD. Biocide use and antibiotic resistance: the relevance of laboratory findings to clinical and environmental situations. Lancet Infect Dis. 2003;3:794–803.

    Article  CAS  Google Scholar 

  3. Thomas L, Russell AD, Maillard J-Y. Antimicrobial activity of chlorhexidine diacetate and benzalkonium chloride against Pseudomonas aeruginosa and its response to biocide residues. J Appl Microbiol. 2005;98:533–43.

    Article  CAS  Google Scholar 

  4. Fernandes P, Ferreira BS, Cabral JM. Solvent tolerance in bacteria: role of efflux pumps and cross-resistance with antibiotics. Int J Antimicrob Agents. 2003;22:211–6.

    Article  CAS  Google Scholar 

  5. Thomas L, Russell AD, Maillard J-Y. Antimicrobial activity of chlorhexidine diacetate and benzalkonium chloride against Pseudomonas aeruginosa and its response to biocide residues. J Appl Microbiol. 2005;98:533–43.

    Article  CAS  Google Scholar 

  6. Langsrud S, Sidhu MS, Heir E, Askild LH. Bacterial disinfectant resistance a challenge for the food industry. Int Biodeterior Biodegrad. 2003;51:283–90.

    Article  CAS  Google Scholar 

  7. Thabit AK, Crandon JL, Nicolau DP. Antimicrobial resistance: impact on clinical and economic outcomes and the need for new antimicrobials. Expert Opin Pharmacother. 2015;16:159–77.

    Article  CAS  Google Scholar 

  8. Moremi N, Claus H, Mshana SE. Antimicrobial resistance pattern: a report of microbiological cultures at a tertiary hospital in Tanzania. BMC Infect Dis. 2016;16:756.

    Article  Google Scholar 

  9. Owens RC Jr. Antimicrobial stewardship: concepts and strategies in the 21st century. Diagn Microbiol Infect Dis. 2008;61:110–28.

    Article  Google Scholar 

  10. Sievert DM, Ricks P, Edwards JR, Schneider A, Patel J, Srinivasan A, et al. Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009–10. Infect Control Hosp Epidemiol. 2013;34:1–14.

    Article  Google Scholar 

  11. Davin-Regli A, Pagès JM. Cross-resistance between biocides and antimicrobials: an emerging question. Rev Sci Tech. 2012;31:89–104.

    CAS  PubMed  Google Scholar 

  12. Lavilla Lerma L, Benomar N, Casado Muñoz Mdel C, Gálvez A, Abriouel H. Correlation between antibiotic and biocide resistance in mesophilic and psychrotrophic Pseudomonas spp. isolated from slaughterhouse surfaces throughout meat chain production. Food Microbiol. 2015;51:33–44.

    Article  CAS  Google Scholar 

  13. Gilbert P, McBain AJ, Bloomfield SF. Biocide abuse and antimicrobial resistance: being clear about the issues. J Antimicrob Chemother. 2002;50:137–9.

    Article  CAS  Google Scholar 

  14. Gilbert P, McBain AJ. Biocide usage in the domestic setting and concern about antibacterial and antibiotic resistance. J Infect. 2001;43:85–91.

    Article  CAS  Google Scholar 

  15. Lau D, Plotkin BJ. Antimicrobial and biofilm effects of herbs used in traditional Chinese medicine. Nat Prod Commun. 2013;8:1617–20.

    CAS  PubMed  Google Scholar 

  16. Zhang BL, Fan CQ, Dong L, Wang FD, Yue JM. Structural modification of a specific antimicrobial lead against Helicobacter pylori discovered from traditional Chinese medicine and a structure-activity relationship study. Eur J Med Chem. 2010;45:5258–64.

    Article  CAS  Google Scholar 

  17. Wong RWK, Hagg U, Samaranayake L, Yuen MKZ, Seneviratne CJ, Kao R. Antimicrobial activity of Chinese medicine herbs against common bacteria in oral biofilm. A pilot study. Int J Oral Maxillofac Surg. 2010;39:599–605.

    Article  CAS  Google Scholar 

  18. Stermitz FR, Lorenz P, Tawara JN, Zenewicz LA, Lewis K. Synergy in a medicinal plant: antimicrobial action of berberine potentiated by 50-methoxyhydno-carpin, a multidrug pump inhibitor. Proc Natl Acad Sci U S A. 2000;97:1433–7.

    Article  CAS  Google Scholar 

  19. Betoni JE, Mantovani RP, Barbosa LN, Stasi LC, Junior AF. Synergism between plant extract and antimicrobial drugs used on Staphylococcus aureus diseases. Mem Inst Oswaldo Cruz. 2006;101:387–90.

    Article  Google Scholar 

  20. Sibanda T, Okoh AI. The challenges of overcoming antibiotic resistance: plant extracts as potential sources of antimicrobial and resistance modifying agents. Afr J Biotechnol. 2007;6:2886–96.

    Google Scholar 

  21. Choi UK, Kim MH, Lee NH. Optimization of antibacterial activity by Gold-Thread (Coptidis Rhizoma Franch) against Streptococcus mutans using evolutionary operation-factorial design technique. J Microbiol Biotechnol. 2007;17:1880–4.

    PubMed  Google Scholar 

  22. Luo JY, Yan D, Yang MH. Study of the anti-MRSA activity of Rhizoma coptidis by chemical fingerprinting and broth microdilution methods. Chin J Nat Med. 2014;12:393–400.

    CAS  PubMed  Google Scholar 

  23. Wang DW, Liu ZQ, Guo MQ, Liu SY. Structural elucidation and identification of alkaloids in Rhizoma coptidis by electrospray ionization tandem mass spectrometry. J Mass Spectrom. 2004;39:1356–65.

    Article  CAS  Google Scholar 

  24. Yokozawa T, Ishida A, Kashiwada Y, Cho EJ, Kim HY, Ikeshiro Y. Coptidis rhizoma: protective effects against peroxynitrite-induced oxidative damage and elucidation of its active components. J Pharm Pharm. 2004;56:547–56.

    Article  CAS  Google Scholar 

  25. Asai M, Iwata N, Yoshikawa A, Aizaki Y, Ishiura S, Saido TC, et al. Berberine alters the processing of Alzheimer’s amyloid precursor protein to decrease Abeta secretion. Biochem Biophys Res Commun. 2007;352:498–502.

    Article  CAS  Google Scholar 

  26. Wen SQ, Jeyakkumar P, Avula SR, Zhang L, Zhou CH. Discovery of novel berberine imidazoles as safe antimicrobial agents by down regulating ROS generation. Bioorg Med Chem Lett. 2016;26:2768–73.

    Article  CAS  Google Scholar 

  27. Wu DM, Lu RC, Chen YQ, Qiu J, Deng CC, Tan Q. Study of cross-resistance mediated by antibiotics, chlorhexidine and Rhizoma coptidis in Staphylococcus aureus. J Glob Antimicrob Resist. 2016;7:61–6.

    Article  Google Scholar 

  28. Chinese Pharmacopoeia Commission. Pharmacopoeia of the People’s Republic of China (Part 2). Beijing, China: China Medical Science Press; 2010, p. 213–4.

  29. Blaszczyk T, Krzyzanowska J, Lamer-Zarawska E. Screening for antimycotic properties of 56 traditional Chinese drugs. Phytother Res. 2000;14:210–2.

    Article  CAS  Google Scholar 

  30. Kong WJ, Zhao YL, Xiao XH, Wang JB, Li HB, Li ZL, et al. Spectrum–effect relationships between ultra-performance liquid chromatography fingerprints and antibacterial activities of Rhizoma coptidis. Anal Chim Acta. 2009;634:279–85.

    Article  CAS  Google Scholar 

  31. European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 9.0, 2019. http://www.eucast.org.

  32. Dos Santos HRM, Argolo CS, Argolo-Filho RC, Loguercio LL. A 16S rDNA PCR-based theoretical to actual delta approach on culturable mock communities revealed severe losses of diversity information. BMC Microbiol. 2019;19:74.

    Article  Google Scholar 

  33. Kanehisa M. The KEGG database. Novartis Found Symp. 2002;247:91–101.

  34. Qian Y, Linglin G, Teng X, Yun C, Xin Y, Mengmeng H, et al. Amoxicillin administration regimen and resistance mechanisms of staphylococcus aureus established in tissue cage infection model. Front Microbiol. 2019;10:1–9.

    Google Scholar 

  35. Grossman TH. Tetracycline antibiotics and resistance. Cold Spring Harb Perspect Med. 2016. https://doi.org/10.1101/cshperspect.a025387.

  36. Wencewicz TA. Crossroads of antibiotic resistance and biosynthesis. J Mol Biol. 2019;431:3370–99.

    Article  CAS  Google Scholar 

  37. Favrot L, Blanchard JS, Vergnolle O. Bacterial GCN5-related N-acetyltransferases: from resistance to regulation. Biochemistry. 2016;55:989–1002.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful for Professor Xian Zhang for kindly providing the clinical isolates.

Funding

This study was supported by Natural Science Foundation of Guangxi Autonomous Region (NO. 2014GXNSFAA118176), Development and Research Center for China-ASEAN Traditional Medicine and Nanning City Science and Technology Plan [NO. 20131062].

Author information

Authors and Affiliations

  1. Institute of Pharmacy, Guangxi University of Chinese Medicine, Nanning, Guangxi, PR China

    Sugui Lan, Zhirong Li, Aiqiu Su, Yanhong Peng, Yanke Liao, Xuemei Liu & Qiang Tan

Authors
  1. Sugui Lan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhirong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aiqiu Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yanhong Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yanke Liao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xuemei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qiang Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qiang Tan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

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

Lan, S., Li, Z., Su, A. et al. Study on the mechanisms of the cross-resistance to TET, PIP, and GEN in Staphylococcus aureus mediated by the Rhizoma Coptidis extracts. J Antibiot 74, 330–336 (2021). https://doi.org/10.1038/s41429-021-00407-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41429-021-00407-4

Search

Advanced search

Quick links