Effects of Cuts and Different Phenological Stages on Antibacterial and Antioxidant Activities and Chemical Attributes of Garden Thyme (Thymus vulgaris L.) Essential Oil

Yıl 2021, Cilt: 31 Sayı: 3, 663 - 677, 15.09.2021

Reza Pourabdal Latifeh Pourakbar Amir Rahimi Amir Tukmechi

https://doi.org/10.29133/yyutbd.839422

Öz

Garden thyme is an aromatic plant with various applications in the pharmaceutical, food, and hygienic-cosmetic industries around the world. In this research, field-cultivated plants were harvested in two cuts and three consecutive stages (pre-flowering, flowering, and post-flowering). The essential oil percentage and compositions were identified in the essential oil samples. The antibacterial activity of the essential oil was measured against Escherichia coli and Staphylococcus aureus. The antioxidant activity, total phenol and flavonoid contents, chain-breaking activity, and IC50 were recorded. The highest essential oil percentage (2.56%) was obtained from the pre-flowering stage. The results of GC/MS revealed that p-cymene, γ-terpinene, thymol, and carvacrol were the most important constituents of the studied essential oil. The lowest antibacterial activity was recorded by the second cut at the pre-flowering stage. The highest antibacterial activity against E. coli and S. aureus were recorded by the second cut during the flowering stage and the first cut during the flowering stage, respectively. The lowest MIC was 15.75 μg mL-1 related to the second cut during the flowering stage. The plants had the highest total phenol (16.64 mg GAE g-1 DM) and total flavonoid contents (2.88 mg QE g-1 DM) at the pre-flowering stage. The highest antioxidant activity (IC50 = 134.05 μg mL-1) was observed at the pre-flowering stage. It can be said that phenological stages and cuts can affect essential oil antibacterial and antioxidant activities, as well as its chemical characteristics.

Anahtar Kelimeler

Antibacterial activity, Antioxidant activity, Cut, Essential oil, Garden thyme, Phenological periods

Kesimlerin ve Farklı Fenolojik Aşamaların Bahçe Kekiği (Thymus vulgaris L.) Uçucu Yağının Antibakteriyel ve Antioksidan Aktiviteleri ve Kimyasal Özellikleri Üzerine Etkileri

Öz

Bahçe kekiği, dünya çapında ilaç, gıda ve hijyenik-kozmetik endüstrilerinde çeşitli uygulamalara sahip aromatik bir bitkidir. Bu araştırmada, tarlada yetiştirilen bitkiler iki kesimde ve birbirini takip eden üç aşamada (çiçeklenme öncesi, çiçeklenme ve çiçeklenme sonrası) hasat edilmiştir. Uçucu yağ örneklerinde uçucu yağ yüzdesi ve bileşimleri belirlendi. Uçucu yağın antibakteriyel aktivitesi Escherichia coli ve Staphylococcus aureus'a karşı ölçülmüştür. Antioksidan aktivite, toplam fenol ve flavonoid içerikleri, zincir kırma aktivitesi ve IC50 kaydedildi. En yüksek uçucu yağ yüzdesi (%2.56) çiçeklenme öncesi dönemden elde edilmiştir. GC/MS sonuçları, çalışılan uçucu yağın en önemli bileşenlerinin p-cymene, γ-terpinen, timol ve karvakrol olduğunu ortaya koydu. En düşük antibakteriyel aktivite, çiçeklenme öncesi aşamadaki ikinci kesimde kaydedilmiştir. E. coli ve S. aureus'a karşı en yüksek antibakteriyel aktivite, sırasıyla çiçeklenme döneminde ikinci kesimde ve çiçeklenme döneminde ilk kesimde kaydedilmiştir. En düşük MIC, çiçeklenme döneminde ikinci kesime bağlı olarak 15.75 μg mL-1 idi. Bitkiler, çiçeklenme öncesi aşamada en yüksek toplam fenol (16.64 mg GAE g-1 DM) ve toplam flavonoid içeriğine (2.88 mg QE g-1 DM) sahipti. En yüksek antioksidan aktivite (IC50 = 134.05 μg mL-1) çiçeklenme öncesi aşamada gözlenmiştir. Fenolojik aşamaların ve kesimlerin uçucu yağın kimyasal özelliklerinin yanı sıra antibakteriyel ve antioksidan aktivitelerini de etkileyebileceği söylenebilir.

Anahtar Kelimeler

Antibakteriyel aktivite, Antioksidan aktivite, Kesmek, Esans, Bahçe kekiği, Fenolojik dönemler.

Kaynakça

• 1. Andrade-Ochoa, S., Nevárez-Moorillón, G. V., Sánchez-Torres, L. E., Villanueva-García, M., Sánchez-Ramírez, B. E., Rodríguez-Valdez, L. M., & Rivera-Chavira, B. E. (2015). Quantitative structure-activity relationship of molecules constituent of different essential oils with antimycobacterial activity against Mycobacterium tuberculosis and Mycobacterium bovis. BMC complementary and alternative medicine, 15(1), 332.
• 2. Bensouilah J, Buck P (2006) Aromadermatology: Aromatherapy in the Treatment and Care of Common Skin Conditions. Radcliffe,
• 3. Brand-Williams, W., Cuvelier, M. E., & Berset, C. L. W. T. (1995). Use of a free radical method to evaluate antioxidant activity. LWT-Food science and Technology, 28(1), 25-30.
• 4. Casiglia S, Bruno M, Scandolera E, Senatore F, Senatore F (2015) Influence of harvesting time on composition of the essential oil of Thymus capitatus (L.) Hoffmanns. & Link. growing wild in northern Sicily and its activity on microorganisms affecting historical art crafts Arabian Journal of Chemistry doi:https://doi.org/10.1016/j.arabjc.2015.05.017
• 5. Cosentino, S. C. I. G., Tuberoso, C. I. G., Pisano, B., Satta, M. L., Mascia, V., Arzedi, E., & Palmas, F. (1999). In‐vitro antimicrobial activity and chemical composition of Sardinian thymus essential oils. Letters in applied microbiology, 29(2), 130-135.
• 6. Cristani, M., D'Arrigo, M., Mandalari, G., Castelli, F., Sarpietro, M. G., Micieli, D., ... & Trombetta, D. (2007). Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity. Journal of agricultural and food chemistry, 55(15), 6300-6308.
• 7. Dahham, S. S., Tabana, Y. M., Iqbal, M. A., Ahamed, M. B., Ezzat, M. O., Majid, A. S., & Majid, A. M. (2015). The anticancer, antioxidant and antimicrobial properties of the sesquiterpene β-caryophyllene from the essential oil of Aquilaria crassna. Molecules, 20(7), 11808-11829.
• 8. Delgado, T., Marinero, P., Manzanera, M. C. A. S., Asensio, C., Herrero, B., Pereira, J. A., & Ramalhosa, E. (2014). Antioxidant activity of twenty wild Spanish Thymus mastichina L. populations and its relation with their chemical composition. LWT-Food Science and Technology, 57(1), 412-418.
• 9. Duda, S. C., Mărghitaş, L. A., Dezmirean, D., Duda, M., Mărgăoan, R., and Bobiş, O., Changes in major bioactive compounds with antioxidant activity of Agastache foeniculum, Lavandula angustifolia, Melissa officinalis and Nepeta cataria: Effect of harvest time and plant species, Industrial Crops and Products., 2015, vol. 77, p. 499-507
• 10. Fatma G, Mouna BF, Mondher M, Ahmed L (2014) In-vitro assessment of antioxidant and antimicrobial activities of methanol extracts and essential oil of Thymus hirtus sp. algeriensis Lipids Health Dis 13:114-114 doi:10.1186/1476-511X-13-114
• 11. Fournomiti M et al. (2015) Antimicrobial activity of essential oils of cultivated oregano (Origanum vulgare), sage (Salvia officinalis), and thyme (Thymus vulgaris) against clinical isolates of Escherichia coli, Klebsiella oxytoca, and Klebsiella pneumoniae Microb Ecol Health Dis 26:23289-23289 doi:10.3402/mehd.v26.23289
• 12. Freires IA, Denny C, Benso B, de Alencar SM, Rosalen PL (2015) Antibacterial Activity of Essential Oils and Their Isolated Constituents against Cariogenic Bacteria: A Systematic Review Molecules (Basel, Switzerland) 20:7329-7358 doi:10.3390/molecules20047329
• 13. Galeotti, F., Barile, E., Curir, P., Dolci, M., & Lanzotti, V. (2008). Flavonoids from carnation (Dianthus caryophyllus) and their antifungal activity. Phytochemistry Letters, 1(1), 44-48.
• 14. Gedikoğlu, A., Sökmen, M., & Çivit, A. (2019). Evaluation of Thymus vulgaris and Thymbra spicata essential oils and plant extracts for chemical composition, antioxidant, and antimicrobial properties. Food science & nutrition, 7(5), 1704-1714.
• 15. Ghasemi Pirbalouti, A., & Gholipour, Z. (2016). Chemical composition, antimicrobial and antioxidant activities of essential oil from Echinophora cinerea harvested at two phenological stages. Journal of EssEntial oil rEsEarch, 28(6), 501-511.
• 16. Göçer, H., & Gülçin, İ. (2011). Caffeic acid phenethyl ester (CAPE): correlation of structure and antioxidant properties. International journal of food sciences and nutrition, 62(8), 821-825.
• 17. Jordán, M. J., Lax, V., Rota, M. C., Lorán, S., & Sotomayor, J. A. (2013). Effect of the phenological stage on the chemical composition, and antimicrobial and antioxidant properties of Rosmarinus officinalis L essential oil and its polyphenolic extract. Industrial Crops and Products, 48, 144-152.
• 18. Kavoosi, G., Dadfar, S. M. M., & Purfard, A. M. (2013). Mechanical, physical, antioxidant, and antimicrobial properties of gelatin films incorporated with thymol for potential use as nano wound dressing. Journal of Food Science, 78(2), E244-E250.
• 19. Köksal, E., Bursal, E., Gülçin, İ., Korkmaz, M., Çağlayan, C., Gören, A. C., & Alwasel, S. H. (2017). Antioxidant activity and polyphenol content of Turkish thyme (Thymus vulgaris) monitored by liquid chromatography and tandem mass spectrometry. International Journal of Food Properties, 20(3), 514-525.
• 20. Kordali S, Cakir A, Ozer H, Cakmakci R, Kesdek M, Mete E (2008) Antifungal, phytotoxic and insecticidal properties of essential oil isolated from Turkish Origanum acutidens and its three components, carvacrol, thymol and p-cymene Bioresource Technology 99:8788-8795 doi:https://doi.org/10.1016/j.biortech.2008.04.048
• 21. Kouidhi B, Al Qurashi YMA, Chaieb K (2015) Drug resistance of bacterial dental biofilm and the potential use of natural compounds as alternative for prevention and treatment Microbial Pathogenesis 80:39-49 doi:https://doi.org/10.1016/j.micpath.2015.02.007
• 22. Kovač, J., Šimunović, K., Wu, Z., Klančnik, A., Bucar, F., Zhang, Q., & Možina, S. S. (2015). Antibiotic resistance modulation and modes of action of (-)-α-pinene in Campylobacter jejuni. PloS one, 10(4). linalool and α-terpineol against periodontopathic and cariogenic bacteria. Anaerobe, 18(3), 369-372.
• 23. Mahboubi, M., & Kazempour, N. (2011). Chemical composition and antimicrobial activity of Satureja hortensis and Trachyspermum copticum essential oil. Iranian journal of microbiology, 3(4), 194.
• 24. Martins, N., Barros, L., Santos-Buelga, C., Silva, S., Henriques, M., & Ferreira, I. C. (2015). Decoction, infusion and hydroalcoholic extract of cultivated thyme: Antioxidant and antibacterial activities, and phenolic characterisation. Food chemistry, 167, 131-137.
• 25. McGimpsey, J. A., Douglas, M. H., Van Klink, J. W., Beauregard, D. A., & Perry, N. B. (1994). Seasonal variation in essential oil yield and composition from naturalized Thymus vulgaris L. in New Zealand. Flavour and Ragrance Journal, 9(6), 347-352.‏
• 26. Miladi H, Slama R, Mili D, Zouari S, Bakhrouf A, Ammar E (2013) Essential oil of Thymus vulgaris L. and Rosmarinus officinalis L.: Gas chromatography-mass spectrometry analysis, cytotoxicity and antioxidant properties and antibacterial activities against foodborne pathogens Natural Science 05:729-739 doi:10.4236/ns.2013.56090
• 27. Mitropoulou, G., Fitsiou, E., Stavropoulou, E., Papavassilopoulou, E., Vamvakias, M., Pappa, A., ... & Kourkoutas, Y. (2015). Composition, antimicrobial, antioxidant, and antiproliferative activity of Origanum dictamnus (dittany) essential oil. Microbial ecology in health and disease, 26(1), 26543.
• 28. Morshedloo, M. R., Mumivand, H., Craker, L. E., & Maggi, F. (2018). Chemical composition and antioxidant activity of essential oils in Origanum vulgare subsp. gracile at different phenological stages and plant parts. Journal of Food Processing and Preservation, 42(2), e13516.
• 29. Morteza-Semnani, K., Rostami, B., & Akbarzadeh, M. (2006). Essential oil composition of Thymus kotschyanus and Thymus pubescens from Iran. Journal of Essential Oil Research, 18(3), 272-274.
• 30. Nadia, Z., & Rachid, M. (2013). Antioxidant and antibacterial activities of Thymus vulgaris L. Medicinal and Aromatic Plant Research Journal, 1(1), 5-11.
• 31. Nedorostova L, Kloucek P, Kokoska L, Stolcova M, Pulkrabek J (2009) Antimicrobial properties of selected essential oils in vapour phase against foodborne bacteria Food Control 20:157-160 doi:https://doi.org/10.1016/j.foodcont.2008.03.007
• 32. Oki, T., Masuda, M., Furuta, S., Nishiba, Y., Terahara, N., & Suda, I. (2002). Involvement of anthocyanins and other phenolic compounds in radical‐scavenging activity of purple‐fleshed sweet potato cultivars. Journal of Food Science, 67(5), 1752-1756.
• 33. Park, S. N., Lim, Y. K., Freire, M. O., Cho, E., Jin, D., & Kook, J. K. (2012). Antimicrobial effect of
• 34. Parsaeimehr, M., Basti, A. A., Radmehr, B., Misaghi, A., Abbasifar, A., Karim, G., ... & Khanjari, A. (2010). Effect of Zataria multiflora boiss. Essential oil, nisin, and their combination on the production of enterotoxin C and α-hemolysin by Staphylococcus aureus. Foodborne pathogens and disease, 7(3), 299-305.
• 35. Pasqua R, De Feo V, Villani F, Mauriello G (2005) In vitro antibacterial activity of essential oil from Mediterranean Apiaceae, Verbenaceae and Lamiaceae against foodborne pathogens and spoilage bacteria Annals of Microbiology 55:139-143
• 36. Pattnaik, S., Subramanyam, V. R., Bapaji, M., & Kole, C. R. (1997). Antibacterial and antifungal activity of aromatic constituents of essential oils. Microbios, 89(358), 39-46.
• 37. Qaiyami S. (2007). Macro- and microdilution methods of antimicrobial suscebtibility testing. In:"Antimicrobial suscebtibility testing protocols, (Schwalbe R, Steele-Moore L, Goodwin AC.Eds.)", Taylor & francis Group, New York,USA, pp. 75-81.
• 38. Rojas-Graü MA et al. (2007) Effects of plant essential oils and oil compounds on mechanical, barrier and antimicrobial properties of alginate–apple puree edible films Journal of Food Engineering 81:634-641 doi:https://doi.org/10.1016/j.jfoodeng.2007.01.007
• 39. Roldán LP, Díaz GJ, Duringer JM (2010) Composition and antibacterial activity of essential oils obtained from plants of the Lamiaceae family against pathogenic and beneficial bacteria Revista Colombiana de Ciencias Pecuarias 23:451-461
• 40. Rota MC, Herrera A, Martínez RM, Sotomayor JA, Jordán MJ (2008) Antimicrobial activity and chemical composition of Thymus vulgaris, Thymus zygis and Thymus hyemalis essential oils Food Control 19:681-687 doi:https://doi.org/10.1016/j.foodcont.2007.07.007
• 41. Salehi, S., Golparvar, A. R., & Hadipanah, A. (2014). Effect of harvest time on yield and quality of Thymus vulgaris L. essential oil in Isfahan province, Iran. Agriculturae Conspectus Scientificus, 79(2), 115-118.
• 42. Saoud I et al. (2013) Journal Article Acta Alimentaria, Volume 42, Number 3/September 2013 Chemical composition, weed killer and antifungal activities of Tunisian thyme (Thymus capitatus Hoff. et Link.) essential oils Acta Alimentaria 42:417-427 doi:10.1556/AAlim.42.2013.3.15
• 43. Sarikurkcu C, Tepe B, Daferera D, Polissiou M, Harmandar M (2008) Studies on the antioxidant activity of the essential oil and methanol extract of Marrubium globosum subsp. globosum (lamiaceae) by three different chemical assays Bioresource Technology 99:4239-4246 doi:https://doi.org/10.1016/j.biortech.2007.08.058
• 44. Sartoratto A, Machado A, Delarmelina C, Figueira G, Duarte M, Rehder V (2004) Composition and antimicrobial activity of essential oils from aromatic plants used in Brazil Brazilian Journal of Microbiology - BRAZ J MICROBIOL 35 doi:10.1590/S1517-83822004000300001
• 45. Sefidkon, F., & Akbari-nia, A. (2009). Essential oil content and composition of Satureja sahendica Bornm. at different stages of plant growth. Journal of Essential Oil Research, 21(2), 112-114.
• 46. Serra Bonvehi, J., Soliva Torrentó, M., & Centelles Lorente, E. (2001). Evaluation of polyphenolic and flavonoid compounds in honeybee-collected pollen produced in Spain. Journal of agricultural and food chemistry, 49(4), 1848-1853.
• 47. Sokovic, M., Petar D. Marin, Dejan Brkic, and Leo JLD van Griensven. "Chemical composition and antibacterial activity of essential oils against human pathogenic bacteria." Food 1, no. 2 (2008): 220-226.
• 48. Tardugno R, Pellati F, Iseppi R, Bondi M, Bruzzesi G, Benvenuti S (2018) Phytochemical composition and in vitro screening of the antimicrobial activity of essential oils on oral pathogenic bacteria Natural Product Research 32:544-551 doi:10.1080/14786419.2017.1329730
• 49. Toncer, O., Karaman, S., Diraz, E., Sogut, T., & Kizil, S. (2017). Essential oil composition of Thymus× citriodorus (Pers.) Schreb. at different harvest stages. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 45(1), 185-189.
• 50. Tripoli, E., La Guardia, M., Giammanco, S., Di Majo, D., & Giammanco, M. (2007). Citrus flavonoids: Molecular structure, biological activity and nutritional properties: A review. Food chemistry, 104(2), 466-479.
• 51. WESOLOWSKA, A., & JADCZAK, D. (2019). Comparison of the Chemical Composition of Essential Oils Isolated from Two Thyme (Thymus vulgaris L.) Cultivars. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 47(3).
• 52. Zantar, S., El Garrouj, D., Pagán, R., Chabi, M., Laglaoui, A., Bakkali, M., & Zerrouk, M. H. (2015). Effect of harvest time on yield, chemical composition, antimicrobial and antioxidant activities of Thymus vulgaris and Mentha pulegium essential oils. European Journal of Medicinal Plants, 69-77.