Aromatherapeutic essential oils and their pharmaceutical combinations: Tools for inhibition of quorum sensing activity and biofilm formation of human pathogens*

Abstract

Background and Aims: Aromatherapy, as one of the complementary therapies, uses essential oils as the main therapeutic agents to treat several diseases. In the present study, it was aimed to investigate inhibition of quorum sensing (QS) and bio- film formation of aromatherapeutic essential oils (AEOs) and their pharmaceutical combinations (PC-I and PC-II).
Methods: The anti-QS potential of AEOs were determined using the biosensor strains Chromobacterium violaceum ATCC 12472 and Pseudomonas aeruginosa PAO1. Anti-QS activity was detected by agar-well diffusion and violacein pigment inhi- bition assays. Blocking of PAO1 swim and swarm motilities and biofilm formation was also performed.
Results: Most of the AEOs demonstrated highly active (>95%) violacein pigment inhibition. Additionally, they inhibited swarming (40.34%-72.80%) and swimming (20.06%-50.08%) motilities of PAO1. Moreover, the majority of AEOs also de- creased the biofilm formation, particularly on P. aeruginosa and S. aureus.
Conclusion: Consequently, aromatherapeutic formulations might be a complementary or prophylactic cure for infectious dis- ease by their anti-QS and antibiofilm activities rather than just antimicrobial effects.

Keywords

• Aromatherapeutic essential oils
• Antibiofilm
• Quorum sensing
• Pseudomonas aeruginosa PAO1
• Synergistic effect

References

1. Ahmad, A., Viljoen, A., & Chenia, H. (2015). The impact of plant volatiles on bacterial quorum sensing. Letters in Applied Microbiol- ogy, 60(1), 8-19. https://doi.org/10.1111/lam.12343
2. Ali, B., Al-Wabel, N. A., Shams, S., Ahamad, A., Khan, S. A., & Anwar,F. (2015). Essential oils used in aromatherapy: A systemic review. Asian Pacific Journal of Tropical Biomedicine, 5(8), 601-611. https:// doi.org/10.1016/j.apjtb.2015.05.007
3. Alibi, S., Selma, W. B., Ramos-Vivas, J., Smach, M. A., Touati, R., Boukadida, J., Navas, J. & Mansour, H. B. (2020). Anti-oxidant, anti- bacterial, anti-biofilm, and anti-quorum sensing activities of four essential oils against multidrug-resistant bacterial clinical isolates. Current Research in Translational Medicine, 68(2), 59-66.https://doi. org/10.1016/j.retram.2020.01.001
4. Bai A, J., & Vittal, R. R. (2014). Quorum sensing inhibitory and anti- biofilm activity of essential oils and their in vivo efficacy in food systems. Food Biotechnology, 28(3), 269-292. https://doi.org/10.1 080/08905436.2014.932287
5. Bharti, S. K., Pathak, V., Alam, T., Arya, A., Singh, V. K., Verma, A. K., & Rajkumar, V. (2020). Materialization of novel composite bio‐based active edible film functionalized with essential oils on antimicro- bial and antioxidative aspect of chicken nuggets during extend- ed storage. Journal of Food Science, 85(9), 2857-2865. https://doi. org/10.1111/1750-3841.15365
6. Blosser, R. S., & Gray, K. M. (2000). Extraction of violacein from Chromobacterium violaceum provides a new quantitative bioas- say for N-acyl homoserine lactone autoinducers. Journal of Micro- biological Methods, 40(1), 47-55. https://doi.org/10.1016/S0167- 7012(99)00136-0
7. Boire, N. A., Riedel, S., & Parrish, N. M. (2013). Essential oils and future antibiotics: new weapons against emerging ‘superbugs’. Journal of Ancient Diseases & Preventive Remedies, 1(2), 1000105. https://doi.org/10.4172/jadpr.1000105
8. Brun, P., Bernabè, G., Filippini, R., & Piovan, A. (2019). In vitro anti- microbial activities of commercially available tea tree (Melaleuca alternifolia) essential oils. Current Microbiology, 76(1), 108-116. https://doi.org/10.1007/s00284-018-1594-x.

9. Bali, E. B., Erkan Türkmen, K. , Erdönmez, D., & Sağlam, N. (2019). Comparative study of inhibitory potential of dietary phytochemi- cals against quorum sensing activity of and biofilm formation by Chromobacterium violaceum 12472, and swimming and swarm- ing behaviour of Pseudomonas aeruginosa PAO1. Food Technol- ogy and Biotechnology, 57(2), 212-221. https://doi.org/10.17113/ ftb.57.02.19.5823
10. Cáceres, M., Hidalgo, W., Stashenko, E., Torres, R., & Ortiz, C. (2020). Essential oils of aromatic plants with antibacterial, anti-biofilm and anti-quorum sensing activities against pathogenic bacteria. Antibiotics, 9(4), 147. https://doi.org/10.3390/antibiotics9040147
11. Doğan, Ş., Gökalsın, B., Şenkardeş, İ., Doğan, A., & Sesal, N. C. (2019). Anti- quorum sensing and anti-biofilm activities of Hypericum perforatum extracts against Pseudomonas aeruginosa. Journal of Ethnopharmacol- ogy, 235, 293-300. https://doi.org/10.1016/j.jep.2019.02.020
12. Eris, R., & Ulusoy, S. (2013). Rose, clove, chamomile essential oils and pine turpentine inhibit quorum sensing in Chromobacterium violaceum and Pseudomonas aeruginosa. Journal of Essential Oil Bearing Plants, 16(2), 126-135. https://doi.org/10.1080/097206 0X.2013.794026
13. Husain, F. M., Ahmad, I., Khan, M. S., Ahmad, E., Tahseen, Q., Khan,M. S., & Alshabib, N. A. (2015). Sub-MICs of Mentha piperita essen- tial oil and menthol inhibits AHL mediated quorum sensing and biofilm of Gram-negative bacteria. Frontiers in Microbiology, 6, 420. https://doi.org/10.3389/fmicb.2015.00420
14. Ilic-Tomić, T., Soković, M., Vojnović, S., Ćirić, A. D., Veljić, M., Nikodinović-Runić, J., & Novaković, M. M. (2017). Diarylheptanoids from Alnus viridis ssp viridis and Alnus glutinosa: Modulation of Quorum Sensing Activity in Pseudomonas aeruginosa. Planta med- ica, 83(01-02), 117-125. https://doi.org/10.1055/s-0042-107674
15. Kavanaugh, N. L., & Ribbeck, K. (2012). Selected antimicrobial essential oils eradicate Pseudomonas spp. and Staphylococcus aureus biofilms. Applied and Environmental Microbiology, 78(11), 4057-4061. https://doi.org/10.1128/AEM.07499-11
16. Kerekes, E. B., Deák, É., Takó, M., Tserennadmid, R., Petkovits, T., Vágvölgyi, C., & Krisch, J. (2013). Anti‐biofilm forming and anti‐ quorum sensing activity of selected essential oils and their main components on food‐related micro‐organisms. Journal of Applied Microbiology, 115(4), 933-942. https://doi.org/10.1111/jam.12289
17. Li, S., Chen, S., Fan, J., Cao, Z., Ouyang, W., Tong, N., Hu, X., Hu, J., Li, P., Feng, Z. & Huang, X. (2018). Anti-biofilm effect of novel thiazole acid analogs against Pseudomonas aeruginosa through IQS path- ways. European Journal of Medicinal Chemistry, 145, 64-73. https:// doi.org/10.1016/j.ejmech.2017.12.076
18. Luís, Â., Duarte, A., Gominho, J., Domingues, F., & Duarte, A. P. (2016). Chemical composition, antioxidant, antibacterial and anti- quorum sensing activities of Eucalyptus globulus and Eucalyptus radiata essential oils. Industrial Crops and Products, 79, 274-282. https://doi.org/10.1016/j.indcrop.2015.10.055
19. Merghni, A., Noumi, E., Hadded, O., Dridi, N., Panwar, H., Ceylan, O., Mastouri, M. & Snoussi, M. (2018). Assessment of the antibiofilm and antiquorum sensing activities of Eucalyptus globulus essen- tial oil and its main component 1, 8-cineole against methicillin- resistant Staphylococcus aureus strains. Microbial Pathogenesis, 118, 74-80. https://doi.org/10.1016/j.micpath.2018.03.006
20. Mokhetho, K. C., Sandasi, M., Ahmad, A., Kamatou, G. P., & Viljoen,A. M. (2018). Identification of potential anti-quorum sensing com- pounds in essential oils: A gas chromatography-based metabo- lomics approach. Journal of Essential Oil Research, 30(6), 399-408. https://doi.org/10.1080/10412905.2018.1503100
21. Mukherji, R., & Prabhune, A. (2014). Novel glycolipids synthesized using plant essential oils and their application in quorum sensing inhibition and as antibiofilm agents. The Scientific World Journal, 2014. https://doi.org/10.1155/2014/890709
22. O’Toole, G. A., & Kolter, R. (1998). Initiation of biofilm forma- tion in Pseudomonas fluorescens WCS365 proceeds via mul- tiple, convergent signalling pathways: a genetic analysis. Molecular Microbiology, 28(3), 449-461. https://doi.org/10.1046/ j.1365-2958.1998.00797.x
23. Oh, S., Yun, W., Lee, J., Lee, C., Kwak, W., & Cho, J. (2017). Effects of es- sential oil (blended and single essential oils) on anti-biofilm forma- tion of Salmonella and Escherichia coli. Journal of Animal Science and Technology, 59(1), 1-5. https://doi.org/10.1186/s40781-017-0127-7
24. Önem, E., Tüzün, B., & Akkoç, S. (2021). Anti-quorum sensing activ- ity in Pseudomonas aeruginos a PA01 of benzimidazolium salts: electronic, spectral and structural investigations as theoretical approach. Journal of Biomolecular Structure and Dynamics, 1-12. https://doi.org/10.1080/07391102.2021.1890222
25. Packiavathy, I. A. S. V., Agilandeswari, P., Musthafa, K. S., Pandian, S. K., & Ravi, A. V. (2012). Antibiofilm and quorum sensing inhibitory potential of Cuminum cyminum and its secondary metabolite methyl eugenol against Gram negative bacterial pathogens. Food Research Interna- tional, 45(1), 85-92. https://doi.org/10.1016/j.foodres.2011.10.022
26. Pellegrini, M. C., Alvarez, M. V., Ponce, A. G., Cugnata, N. M., De Piano, F. G., & Fuselli, S. R. (2014). Anti-quorum sensing and antimi- crobial activity of aromatic species from South America. Journal of Essential Oil Research, 26(6), 458-465. https://doi.org/10.1080/1 0412905.2014.947387
27. Raut, J. S., & Karuppayil, S. M. (2014). A status review on the me- dicinal properties of essential oils. Industrial Crops and Products, 62, 250-264. https://doi.org/10.1016/j.indcrop.2014.05.055
28. Tariq, S., Wani, S., Rasool, W., Shafi, K., Bhat, M. A., Prabhakar, A., Shalla, A.H. & Rather, M.A. (2019). A comprehensive review of the antibacterial, antifungal and antiviral potential of essential oils and their chemical constituents against drug-resistant micro- bial pathogens. Microbial Pathogenesis, 134, 103580.https://doi. org/10.1016/j.micpath.2019.103580
29. Vasavi, H. S., Arun, A. B., & Rekha, P. D. (2014). Anti-quorum sensing activity of Psidium guajava L. flavonoids against Chromobacterium violaceum and Pseudomonas aeruginosa PAO1. Microbiology and Im- munology, 58(5), 286-293. https://doi.org/10.1111/1348-0421.12150
30. Vieira, M., Bessa, L. J., Martins, M. R., Arantes, S., Teixeira, A. P., Mendes, Â., Martins da Costa, P. & Belo, A. D. (2017). Chemical composition, antibacterial, antibiofilm and synergistic proper- ties of essential oils from Eucalyptus globulus Labill. and seven Mediterranean aromatic plants. Chemistry & Biodiversity, 14(6), e1700006. https://doi.org/10.1002/cbdv.201700006
31. Vipin, C., Mujeeburahiman, M., Ashwini, P., Arun, A., & Rekha, P.
32. D. (2019). Anti‐biofilm and cytoprotective activities of quercetin against Pseudomonas aeruginosa isolates. Letters in Applied Mi- crobiology, 68(5), 464-471. https://doi.org/10.1111/lam.13129
33. Yan, M.-R., Wang, C.-H., Cruz Flores, N. J., & Su, Y.-Y. (2019). Targeting open market with strategic business innovations: a case study of growth dynamics in essential oil and aromatherapy industry. Journal of Open Innovation: Technology, Market, and Complexity, 5(1), 7. https://doi.org/10.3390/joitmc5010007
34. Yap, P. S. X., Yiap, B. C., Ping, H. C., & Lim, S. H. E. (2014). Essen- tial oils, a new horizon in combating bacterial antibiotic re- sistance. The Open Microbiology Journal, 8, 6. https://doi. org/10.2174/1874285801408010006
35. Zahin, M., Hasan, S., Aqil, F., Khan, M., Ahmad, S., Husain,F. M., & Ahmad, I. (2010). Screening of certain medicinal plants from India for their anti-quorum sensing activity. http://hdl.handle.net/123456789/10652
36. Zgoda, J., & Porter, J. (2001). A convenient microdilution method for screening natural products against bacteria and fungi. Pharmaceuti- cal Biology, 39(3), 221-225. https://doi.org/10.1076/phbi.39.3.221.5934
37. Zgurskaya, H. I., López, C. A., & Gnanakaran, S. (2015). Perme- ability barrier of Gram-negative cell envelopes and approaches to bypass it. ACS Infectious Diseases, 1(11), 512-522. https://doi. org/10.1021/acsinfecdis.5b00097
38. Zhang, D., Gan, R. Y., Zhang, J. R., Farha, A. K., Li, H. B., Zhu, F., Wang,X.H. & Corke, H. (2020). Antivirulence properties and related mechanisms of spice essential oils: A comprehensive review. Comprehensive Reviews in Food Science and Food Safety, 19(3), 1018-1055. https://doi.org/10.1111/1541-4337.12549
39. Zhang, Y., Djakpo, O., Xie, Y., Guo, Y., Yu, H., Cheng, Y., Qian, H., Shi,R. & Yao, W. (2019). Anti-quorum sensing of Galla chinensis and Coptis chinensis on bacteria. Lebensmittel-Wissenchaft und Tech- nologie, 101, 806-811. https://doi.org/10.1016/j.lwt.2018.11.090
40. Zhang, Y., Kong, J., Xie, Y., Guo, Y., Cheng, Y., Qian, H., & Yao, W. (2018). Essential oil components inhibit biofilm formation in Erwinia caroto- vora and Pseudomonas fluorescens via anti-quorum sensing activ- ity. Lebensmittel-Wissenchaft und Technologie, 92, 133-139. https://doi. org/10.1016/j.lwt.2018.02.027