Skip to main content
SpringerLink
Log in

Biosynthesis of Glycomonoterpenes to Attenuate Quorum Sensing Associated Virulence in Bacteria

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

The acquisition of multidrug resistance in bacteria has become a bigger threat of late, mainly due to the bacterial signaling phenomenon, quorum sensing (QS). QS, among a population of bacteria, initiates the formation of biofilms and offers myriad advantages to bacteria. Burgeoning antibiotic resistance in biofilm-producing bacteria has motivated efforts toward finding new alternatives to these traditional antimicrobials. In the present study, we report the increased solubility and additional quorum quenching as well as biofilm disruption activity of glyco-derivatives of monoterpenes (citral and citronellal). Glycomonoterpenes of citral and citronellal were synthesized via conjugation of the monoterpenes with glucose by the non-pathogenic yeast Candida bombicola (ATCC 22214). Structural elucidation of newly synthesized glycomonoterpenes showed that one synthesized using citronellal contains three major lactonic forms with molecular weight 492.43, 473.47, and 330.39 Da whereas the one produced using citral has an acidic form with molecular weight 389.33 and 346.23 Da. The glycomonoterpenes were able to individually inhibit QS, mediated through various medium-chain and long-chain N-acyl homoserine lactones (AHLs). These new compounds are interesting additions to the known range of quorum sensing inhibitors (QSIs) and could be further explored for potential clinical applications.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Bhardwaj, A. K., Vinothkumar, K., & Rajpara, N. (2013). Bacterial quorum sensing inhibitors: attractive alternatives for control of infectious pathogens showing multiple drug resistance. Recent Patents on Anti-Infective Drug Discovery, 8, 68–83.

    Article  CAS  Google Scholar 

  2. WHO media centre: antimicrobial resistance fact sheets http://www.who.int/mediacentre/factsheets/fs194/en/ Accessed Jan2016.

  3. Mukherji, R., Patil, A., & Prabhune, A. (2015). Role of extracellular proteases in biofilm disruption of gram positive bacteria with special emphasis on Staphylococcus aureus biofilms. Enz Eng, 4, 126. doi:10.4172/2329-6674.1000126.

    Google Scholar 

  4. Heilmann, C., & Götz, F. (2010). Cell–cell communication and biofilm formation in gram-positive bacteria. In R. Krämer & K. Jung (Eds.), Bacterial signaling (pp. 7–17). Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA.

    Google Scholar 

  5. Chen, M., Yu, Q., & Sun, H. (2013). Novel strategies for the prevention and treatment of biofilm related infections. International Journal of Molecular Sciences, 14, 18488–18501.

    Article  Google Scholar 

  6. Kalia, V. C., & Purohit, H. J. (2011). Quenching the quorum sensing system: potential antibacterial drug targets. Critical Reviews in Microbiology, 37, 121–140. doi:10.3109/1040841X.2010.532479.

    Article  CAS  Google Scholar 

  7. Williams, P. (2007). Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology, 153, 3923–3938.

    Article  CAS  Google Scholar 

  8. Kalia VC (2015). Quorum sensing vs quorum quenching: a battle with no end in sight. Springer ISBN 978-81-322-1981-1 DOI 10.1007/978-81-322-1982-8.

  9. Kalia, V. C. (2013). Quorum sensing inhibitors: an overview. Biotechnology Advances, 31, 224–245. doi:10.1016/j.biotechadv.2012.10.004.

    Article  CAS  Google Scholar 

  10. Romero, M., Acuna, L., & Otero, A. (2012). Patents on quorum quenching: interfering with bacterial communication as a strategy to fight infections. Recent Patents on Biotechnology, 6, 2–12. doi:10.2174/187220812799789208.

    Article  CAS  Google Scholar 

  11. LaSarre, B., & Federle, M. J. (2013). Exploiting quorum sensing to confuse bacterial pathogens. Microbiology and Molecular Biology Reviews, 77, 73–111. doi:10.1128/MMBR.00046-12.

    Article  CAS  Google Scholar 

  12. Mukherji, R., & Prabhune, A. (2014). Novel glycolipids synthesized using plant essential oils and their application in quorum sensing inhibition and as antibiofilm agents. Scientific World Journal, 2014, 1–7.

    Article  Google Scholar 

  13. Kerekes, E.-B., Deák, É., Takó, M., Tserennadmid, R., Petkovits, T., Vágvölgyi, C., & Krisch, J. (2013). Anti-biofilm forming and antiquorum sensing activity of selected essential oils and their main components on feed related micro-organisms. Journal of Applied Microbiology, 115, 933–942. doi:10.1111/jam.12289.

    CAS  Google Scholar 

  14. Jesus Olivero-Verbel, Elena E. Stashenko, Irene Wagner-Döbler, and Brigitte Kunze(2011) Anti-quorum sensing activity of essential oils from Colombian plants Natural Product Research Vol. 26, Sensors 2012, 12(4), 4016-4030 doi: 10.1080/14786419.2011.557376.

  15. Ahmad, A., Viljoen, A. M., & Chenia, H. Y. (2015). The impact of plant volatiles on bacterial quorum sensing. Letters in Applied Microbiology, 60, 8–19. doi:10.1111/lam.12343.

    Article  CAS  Google Scholar 

  16. Onawunmi, G. O. (1989). Evaluation of the antimicrobial activity of citral. Lett. Appl. Microbial., 9(3), 105–108. doi:10.1111/j.1472765X.1989.tb00301.x.

  17. Kuwahara, Y., Suzuki, H., Matsumoto, K., & Wada, Y. (1983). Pheromone study on acarid mites. XI. Function of mite body as geometrical isomerization and reduction of citral (the alarm pheromone) Carpoglyphus lactis. Applied Entomology and Zoology, 18, 30–39.

    CAS  Google Scholar 

  18. Robacker, D. C., & Hendry, L. B. (1977). Neral and geranial: components of the sex pheromone of the parasitic wasp, Itoplectis conquisitor. Journal of Chemical Ecology, 3(5), 563–577. doi:10.1007/BF00989077.

    Article  CAS  Google Scholar 

  19. Kim, J. K., Kang, C. S., Lee, J. K., Kim, Y. R., Han, H. Y., & Yun, H. K. (2005). Evaluation of repellency effect of two natural aroma mosquito repellent compounds, citronella and citronellal. Entomological Research, 35(2), 117–120. doi:10.1111/j.17485967.2005.tb00146.x.

    Article  CAS  Google Scholar 

  20. Kazuhiko Nakahara, Najeeb S. Alzoreky, Tadashi Yoshihashi, Huong T. T. Nguyen and Gassinee Trakoontivakorn (2003).Chemical composition and antifungal activity of essential oil from Cymbopogon nardus (citronella grass). JARQ 37 (4).

  21. Rodrigues, L. R., Teixeira, J. A., van der Mei Henny, C., & Oliveira, R. (2006). Physiochemical and functional characterization of a biosurfactant produced by lactococcus lactis 53. Colloids and surfaces. B. Biointerfaces, 49(1), 79–86.

    Article  CAS  Google Scholar 

  22. Dubey, P., Selvaraj, K., & Prabhune, A. (2014). Physico-chemical, analytical and antimicrobial studies of novel sophorolipids synthesized using cetyl alcohol. World journal of pharmacy and pharmaceutical sciences, 3(3), 993–1010.

    CAS  Google Scholar 

  23. Mukherji, R., & Prabhune, A. (2015). A new class of bacterial quorum sensing antagonists: glycomonoterpenols synthesized using linalool and alpha terpineol. World Journal of Microbiology and Biotechnology, 31, 841–849. doi:10.1007/s11274-015-1822-5.

    Article  CAS  Google Scholar 

  24. Lade, H., Paul, D., & Kweon, J. H. (2014). Review Article N-Acyl homoserine lactone-mediated quorum sensing with special reference to use of quorum quenching bacteria in membrane biofouling control. BioMed Research International, 2014(162584), 25.

    Google Scholar 

  25. Hafizah Y. Chenia (2013). Anti-Quorum Sensing Potential of Crude Kigelia africana Fruit Extracts Sensors. 13, 2802-2817; doi:10.3390/s130302802.

  26. Gowrishankar, S., Mosioma, N. D., & Pandian, S. K. (2012). Coral-associated bacteria as a promising antibiofilm agent against methicillin-resistant and -susceptible Staphylococcus aureus biofilms. Evidence-based Complementary and Alternative Medicine, 2012(862374), 16. doi:10.1155/2012/862374.

    Google Scholar 

  27. Packiavathy, I. A. S. V., Priya, S., Pandian, S. K., & Ravi, A. V. (2014). Inhibition of biofilm development of uropathogens by curcumin—an anti-quorum sensing agent from Curcuma longa. Food Chemistry, 148, 453–460.

    Article  CAS  Google Scholar 

  28. Alasil, S. M., Omar, R., Ismail, S., & Yusof, M. Y. (2015). Inhibition of quorum sensing-controlled virulence factors and biofilm formation in Pseudomonas aeruginosa by culture extract from novel bacterial species of Paenibacillus using a rat model of chronic lung infection. International Journal of Bacteriology, 2015(671562), 16. doi:10.1155/2015/671562.

    Google Scholar 

  29. The guardian-antibiotics: http://www.theguardian.com/society/2014/dec/11/drug-resistant-infections-deaths-soar-10m-by-2050-report Accessed May 20, 2016.

  30. Frieden, T. (2013). Antibiotic resistance threats. Cdc 22–50. doi:CS239559-B http://www.cdc.gov/drugresistance/threat-report-2013/ Accessed May 18, 2016.

Download references

Acknowledgments

Amrita Patil thanks UGC for the Ph.D. fellowship and AcSIR for Ph.D. registration.

Author information

Authors and Affiliations

  1. Biochemistry Division, CSIR, National Chemical Laboratory, Dr. Homi Bhabha Road, Pune, 411008, India

    Amrita Patil, Kasturi Joshi-Navre, Ruchira Mukherji & Asmita Prabhune

Authors
  1. Amrita Patil
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kasturi Joshi-Navre
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ruchira Mukherji
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Asmita Prabhune
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Asmita Prabhune.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Supplementary material

Fig. 1 (DOCX 426 kb).

Supplementary material

Fig. 2 (DOCX 608 kb).

Supplementary material

Fig. 3 (DOCX 1251 kb).

Supplementary material

Fig. 4 (DOCX 43 kb).

Supplementary material

Fig. 5 (DOCX 62 kb).

Supplementary material

Fig. 6 (DOCX 639 kb).

Supplementary material

Fig. 7 (DOCX 225 kb).

Supplementary material

Fig. 8 (DOCX 238 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Patil, A., Joshi-Navre, K., Mukherji, R. et al. Biosynthesis of Glycomonoterpenes to Attenuate Quorum Sensing Associated Virulence in Bacteria. Appl Biochem Biotechnol 181, 1533–1548 (2017). https://doi.org/10.1007/s12010-016-2300-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-016-2300-8

Keywords

Search

Navigation