Antimicrobial properties of essential oil of the Monarda L. and its main components

The purpose of this study was to identify the relationship between the antimicrobial activity of extracts and the component composition of essential oils from plant materials Monarda fistulosa L., M. didyma L. and M. x hybrida hort. It was found that the mass fraction of essential oil in dry raw materials of the studied species is 2.49-2.50%, monoterpene phenols (thymol and carvacrol) and monocyclic monoterpenes (γ-terpinene and pcymene) predominate in it. The main components of the essential oil of M. fistulosa are thymol (mass fraction 60.95%) and γ-terpinene (16.6%), M. didyma – γ-terpinene (46.18%), thymol (18.73%), p-cymene (15.07%), M. x hybrida – carvacrol (28.83%), p-cymene (22.90%) thymol (22.85%). The results of the study of the antimicrobial activity of aqueous and alcoholic extracts from plant raw materials of the studied species on natural luminous bacteria Aliivibrio fischeri F1 and the recombinant strain Escherichia coli MG1655 (pXen-lux) showed that M. x hybrida extracts have high antimicrobial activity, which, in our opinion, can be explained by the accumulation of essential oil with a high content of thymol and carvacrol in the aboveground mass of this species, the antibacterial effect of which, according to literary data (Lapina et al., 2018; Dukhanina et al., 2019) consists in the destruction of the cytoplasmic membrane, which increases its permeability and depolarizes its potential, as well as the presence of thymohydroquinone (3.21%), which causes the antitumor effect. The obtained results indicate the potential of using M. x hybrida raw materials for the creation of herbal preparations with antimicrobial, anti-inflammatory, and regenerative activity.

1. Гавриченко Ю.Ю., Сафронюк С.Л., Кацев А.М., Шевчук О.М., Логвиненко Л.А., Феськов С.А. Скрининг антимикробной активности водных и спиртовых извлечений из растительного сырья с использованием биолюминесцентных бактерий // Вестник Воронежского государственного университета. 2022. № 1. С. 60-69. [Gavrichenko Yu.Yu., Safronyuk S.L., Katsev A.M., Shevchuk O.M., Logvinenko L.A., Feskov S.A. Screening of antimicrobial activity of aqueous and alcoholic extracts from plant raw materials using bioluminescent bacteria // Bulletin of the Voronezh State University. 2022. No.1. P. 60-69.]

2. Духанина И.В., Никитина А.С., Никитина Н.В., Феськов С.А., Романов В.А. Обоснование антибактериального действия стоматологических гелей на основе Monarda fistulosa L. экстракта жидкого // Вопросы биологической, медицинской и фармацевтической химии. 2019. 22(1). P. 48-53. doi: 10.29296/25877313-2019-01-07 [Dukhanina I.V., Nikitina A.S., Nikitina N.V., Feskov S.A., Romanov V.A. Justification of the antibacterial action of dental gels based on Monarda fistulosa L. liquid extract // Questions of biological, medical and pharmaceutical chemistry. 2019. 22(1). P. 48-53. DOI: 10.29296/25877313-2019-01-07]

3. Кисленко В.Н., Реймер В.А., Черемушкина В.А., Высочина Г.И. и др. Некоторые фармакологические свойства монарды дудчатой и солянки холмовой // Вестник Новосибирского государственного аграрного университета. 2011. Т. 2. № 18. С. 87-91. [Kislenko V.N., Reimer V.A., Cheremushkina V.A., Vysochina G.I. et al. Some pharmacological properties of Monarda fistulosa and Salsola collina // Bulletin of the Novosibirsk State Agrarian University. 2011. Vol. 2. No. 18. P. 87-91.]

4. Лапина А.С., Варина Н.Р., Куркин В.А., Владимировна А.Е. и др. Монарда дудчатая как перспективный источник получения лекарственных препаратов // Сборник научных трудов ГНБС. 2018. Том 146. С. 175-178. [Lapina A.S., Varina N.R., Kurkin V.A., Vladimirovna A.E. et al. Monarda fistulosa as a promising source for obtaining medicinal products // Collection of scientific papers of the SNBG. 2018. Vol. 146. P. 175-178.]

5. Никитина А.С., Алиев А.М., Феськов С.А., Никитина Н.В. Компонентный состав эфирного масла травы Monarda fistulosa L. из коллекции Никитского ботанического сада // Химия растительного сырья. 2018. № 2. С. 55-62. DOI: 10.14258/jcprm.2018023295 [Nikitina A.S., Aliev A.M., Feskov S.A., Nikitina N.V. Component composition of the essential oil of the herb Monarda fistulosa L. from the collection of the Nikitsky Botanical Gardens // Chemistry of plant raw materials. 2018. No. 2. P. 55-62. DOI: 10.14258/jcprm.2018023295]

6. Ткачев А.В. Исследование летучих веществ растений. Новосибирск: «Офсет». 2008. 969 с. [Tkachev A.V. Study of plant volatiles. Novosibirsk: "Offset", 2008. 969 p.]

7. Шевчук О.М., Исиков В.П., Логвиненко Л.А. Методологические и методические аспекты интродукции ароматических и лекарственных растений / Под ред. Ю.В. Плугатаря. Симферополь: ИТ «Ареал». 2022. 140 с. [Shevchuk O.M., Isikov V.P., Logvinenko L.A. Methodological and methodical aspects of the introduction and selection of aromatic and medicinal plants / Ed. Yu.V. Plugatar. Simferopol: Arial, 2022. 140 р.]

8. Adams R.P. Identification of essential oil compounds by gas chromatography/quadrupole mass spectroscopy. USA: 4th Edition. Allured Pub. Corp, 2007. 804 p.

9. Aeschbach R., Loliger J., Scott B.C. Antioxidant actions of thymol, carvacrol, 6- gingerol, zingerone and hydroxytyrosol // Food and Chemical Toxicology. 1994. Vol. 1. № 32. P. 31-36.

10. Aznar A., Fernández P.S., Periago P.M., Palop A. Antimicrobial activity of nisin, thymol, carvacrol and cymene against growth of Candida lusitaniae // Food Science and Technology International. 2015. Vol. 21. №1. Р. 72-79. DOI: 10.1177/1082013213514593

11. Burt S.A., Van der Zee R., Koets A.P., de Graaff A.M. et al. Carvacrol induces heat shock protein and inhibits synthesis of flagellin in Escherichia coli O157:H7 // Appl. Environ. Microbiol. 2007. Vol. 73. № 14. Р. 4484-4490. DOI: 10.1128/AEM.00340-07

12. Chami N., Bennis S., Chami F. Study of anticandidal activity of carvacrol and eugenol in vitro and in vivo // Oral Microbiology and Immunology. 2005. Vol. 2. № 20. P. 106-111.

13. Cristani M., D’Arrigo M., Mandalari G., Castelli F. et al. Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity // J. Agric. Food Chem. 2007. Vol. 55(15). Р. 6300-6308. DOI: 10.1021/jf070094x

14. Dorman H.J.D., Deans S.G. Antimicrobial agents from plants: Antibacterial activity of plant volatile oils // J. Appl. Microbiol. 2000. Vol. 88. № 2. P. 308-316. DOI: 10.1046/j.1365-2672.2000.00969.x

15. Gabel C.V., Berg H.C. The speed of the flagellar rotary motor of Escherichia coli varies linearly with proton motive force // Proc. Natl. Acad. Sci. USA. 2003. Vol. 100. № 15. Р. 8748-8751. DOI: 10.1073/pnas.1533395100

16. Gutierrez J., Barry-Ryan C., Bourke P. The anti-microbial efficacy of plant essential oil combinations and interactions with food ingredients // Int. J. Food Microbiol. 2008. Vol. 124. № 1. Р. 91-97. DOI: 10.1016/j.ijfoodmicro.2008.02.028

17. La Storia A., Ercolini D., Marinello F., di Pasqua R., Villani F., Mauriello G. Atomic force microscopy analysis shows surface structure changes in carvacrol-treated bacterial cells // Res. Microbiol. 2011. Vol. 162. № 2. Р. 164-172. DOI: 10.1016/j.resmic.2010.11.006

18. Lambert R.J.W., Skandamis P.N., Coote P.J., Nychas G.J.E. A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol // J. Appl. Microbiol. 2001. Vol. 91. № 3. Р. 453-462. DOI: 10.1046/j.1365-2672.2001.01428.x

19. Liu H., Xu X., Wu R., Bi L., Zhang C., Chen H., Yang Y. Antioral squamous cell carcinoma effects of carvacrol via Inhibiting inflammation, proliferation, and migration related to Nrf2/Keap1 Pathway // Biomed Res Int. 2021. PMID: 34212035. DOI: 10.1155/2021/6616547

20. Mastelic J., Jerkovic I., Blazevic I. Comparative study on the antioxidant and biological activities of carvacrol, thymol, and eugenol derivatives // J. of Agricultural and Food Chemistry. 2008. Vol. 1. № 56. P. 3989-3996. DOI: 10.1021/jf073272v

21. Mehdi S.J., Ahmad A., Irshad M. Cytotoxic effect of carvacrol on human cervical cancer cells // Biology and Medicine. 2011. Vol. 2. № 3. P. 307-312. DOI: 10.4172/0974-8369.10000119

22. Mohamed L.S. Immunomodulatory and therapeutic properties of the Nigella sativa L. seed // J. Intern. Immunopharmacology. 2005. №5. P. 1749-1770. DOI: 10.1016/j.intimp.2005.06.008

23. Nazzaro F., Fratianni F., De Martino L., Coppola R., De Feo V. Effect of essential oils on pathogenic bacteria // Pharmaceuticals. 2013. 6. № 12. Р. 1451-1474. DOI: 10.3390/ph6121451

24. Nazzaro F., Fratianni F., d’Acierno A. et al. Essential oils and microbial communication // Essential Oils – Oils of Nature. London. Intech Open. 2020. Р. 1-26. DOI: 10.5772/intechopen.85638.

25. Nychas G.J.E. Natural antimicrobials from plants // New Methods of Food Preservation / Ed. Gould G.W. London: Blackie Academic Professional. 1995. P. 58-89.

26. Ose R., Tu J., Schink A., Maxeiner J., Schuster P. et al. Cinnamon extract inhibits allergen-specific immune responses in human and murine allergy models // Clin. Exp. Allergy. 2020. №50. Р. 41-50. DOI: 10.1111/cea.13507.

27. Thosar N., Basak S., Bahadure R.N., Rajurkar M. Antimicrobial efficacy of five essential oils against oral pathogens: An in vitro study // Eur. J. Dent. 2013. 07(S 01). S071S077. DOI: 10.4103/1305-7456.119078.

28. Sikkema J., de Bont J.A.M., Poolman B. Mechanisms of membrane toxicity of hydrocarbons // Microbiol. Rev. 1995. Vol. 59. № 2. Р. 201-222. DOI: 10.1128/mr.59.2.201222.1995

29. Sobotta L., Lijewski S., Dlugaszewska J. et al. Photodynamic inactivation of Enterococcus faecalis by conjugates of zinc (II) phthalocyanines with thymol and carvacrol loaded into lipid vesicles // Inorganica Chimica Acta. 2019. Vol. 489. P. 180-190. DOI: 10.1016/j.ica.2019.02.031

30. Soković M., Glamočlija J., Marin P.D., Brkić D., van Griensven L.J. Antibacterial effects of the essential oils of commonly consumed medicinal herbs using an in vitro model // Molecules. 2010. Vol. 15. Р. 7532-7546. DOI: 10.3390/molecules15117532.

31. Sovova H., Sajfrtova M., Topiar M. Supercritical CO2 extraction of volatile thymoquinone from Monarda didyma and M. fistulosa herbs // J. Supercrit. Fluids. 2015. Vol. 105. P. 29-34. DOI: 10.1016/j.supflu.2015.01.004.

32. Speranza B., Bevilacqua A., Campaniello D., Altieri C. et al. Minimal inhibitory concentrations of thymol and carvacrol: toward a unified statistical approach to find common trends // Microorganisms. 2023. 11. № 7. Р. 1774-1786. DOI: 10.3390/microorganisms11071774

33. Ultee A., Bennik M.H., Moezelaar R. The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus // Appl. Environ. Microbiol. 2002. Vol. 68. № 4. Р. 1561-1568. DOI: 10.1128/AEM.68.4.1561-1568.2002

34. Zhang L., Gao F., Ge J., Li H., et al. Potential of aromatic plant-derived essential oils for the control of foodborne bacteria and antibiotic resistance in animal production: A review // Antibiotics. 2022. Vol. 11. Р. 1673-1700. DOI: 10.3390/antibiotics11111673.