In vitro Antifungal Activity of Mentha piperita and Thymus vulgaris Essential Oils against Ochratoxigenic Aspergillus carbonarius Isolated from Bozcaada Çavuş Grape

Yıl 2024, Cilt: 34 Sayı: 1, 166 - 175, 31.03.2024

Gülçin Özcan Ateş

https://doi.org/10.29133/yyutbd.1403366

Öz

In this study, the antifungal properties of Mentha piperita and Thymus vulgaris essential oils against an isolate of ochratoxin A producer, Aspergillus carbonarius, isolated from Bozcaada Çavuş grape, were evaluated in three steps. By GC-MS of M. piperita and T. vulgaris essential oils, the main components were determined to be menthol (39.911%) and carvacrol (49.042%). Antifungal activity was first evaluated by the agar well diffusion method, and it was determined that the tested essential oils completely inhibited the growth of A. carbonarius and were as effective as fluconazole antifungal. In the second step, the MIC and MFC values of the tested essential oils were determined; both values were 1 µL mL-1. Finally, it was determined that M. piperita and T. vulgaris essential oils completely inhibited the radial growth of A. carbonarius at the MIC value. These results show that M. piperita and T. vulgaris essential oils may be a good strategy to control ochratoxigenic A. carbonarius contamination.

Anahtar Kelimeler

Antifungal activity, Anti-ochratoxigenic, Aspergillus carbonarius, Mentha piperita, Thymus vulgaris

Destekleyen Kurum

This study was supported by Çanakkale Onsekiz Mart University Scientific Research Projects Coordination Unit with project number FBA-2019-3028.

Proje Numarası

FBA-2019-3028

Teşekkür

In this study, the identification of the isolate was supported by Çanakkale Onsekiz Mart University Scientific Research Projects Coordination with the project number FBA-2019-3028 and the antifungal activity studies were supported by the project number THD-2021-3571. The researcher funded an analysis of the volatile chemical compositions of essential oils. Regarding the use of culture, I would like to thank Dr. Nükhet Nilüfer ZORBA and Dr. Burhan ŞEN. I would like to thank Altın Toroslar A.Ş. (Adana, Türkiye) company for supplying Mentha piperita and Thymus vulgaris essential oils.

Kaynakça

• Achar, P. N., Quyen, P., Adukwu, E. C., Sharma, A., Msimanga, H. Z., Nagaraja, H., & Sreenivasa, M. Y. (2020). Investigation of the antifungal and anti-aflatoxigenic potential of plant-based essential oils against Aspergillus flavus in peanuts. Journal of Fungi, 6(4), 383. https://doi.org/10.3390/jof6040383
• Ambindei, W. A., Jazet, P. M. D., Tatsadjieu, L. N., Priya, P., Manilal, V. B., Krishnakumar, B., & Zollo, P. H. A. (2017). Effect of the essential oils of Thymus vulgaris, Cinnamomum zeylanicum and Mentha piperita on fungal growth and morphology. African Journal of Biotechnology, 16(9), 388-399. https://doi.org/10.5897/AJB2017.15881
• Beigi, M., Torki-Harchegani, M., & Ghasemi Pirbalouti, A. (2018). Quantity and chemical composition of essential oil of peppermint (Mentha× piperita L.) leaves under different drying methods. International Journal of Food Properties, 21(1), 267-276. https://doi.org/10.1080/10942912.2018.1453839
• Bouderba, N. N., Elhussain, K. M. K., & Kadi, H. (2020). In-Vitro Antifungal Activity of Citrullus Colocynthis Schard Against Aflatoxigenic Aspergillus Flavus and Ochratoxigenic Aspergillus Ochraceus. Biomed. J. Sci. Tech. Res, 26, 19759-19764. http://dx.doi.org/10.26717/BJSTR.2020.26.004316
• Boukaew, S., Prasertsan, P., & Sattayasamitsathit, S. (2017). Evaluation of antifungal activity of essential oils against aflatoxigenic Aspergillus flavus and their allelopathic activity from fumigation to protect maize seeds during storage. Industrial Crops and Products, 97, 558-566. https://doi.org/10.1016/j.indcrop.2017.01.005
• Camele, I., Gruľová, D., & Elshafie, H. S. (2021). Chemical composition and antimicrobial properties of Mentha× piperita cv. ‘Kristinka’essential oil. Plants, 10(8), 1567. https://doi.org/10.3390/plants10081567
• Chiotta, M. L., Ponsone, M. L., Sosa, D. M., Combina, M., & Chulze, S. N. (2013). Biodiversity of Aspergillus section Nigri populations in Argentinian vineyards and ochratoxin A contamination. Food Microbiology, 36(2), 182-190. https://doi.org/10.1016/j.fm.2013.04.003
• Císarová, M., Tančinová, D., & Medo, J. (2016). Antifungal activity of lemon, eucalyptus, thyme, oregano, sage and lavender essential oils against Aspergillus niger and Aspergillus tubingensis isolated from grapes. Potravinarstvo, 10(1), 83-88. https://doi.org/10.5219/554
• Dammak, I., Hamdi, Z., El Euch, S. K., Zemni, H., Mliki, A., Hassouna, M., & Lasram, S. (2019). Evaluation of antifungal and anti-ochratoxigenic activities of Salvia officinalis, Lavandula dentata and Laurus nobilis essential oils and a major monoterpene constituent 1, 8-cineole against Aspergillus carbonarius. Industrial Crops and Products, 128, 85-93. https://doi.org/10.1016/j.indcrop.2018.11.006
• Dammak, I., Lasram, S., Hamdi, Z., Moussa, O. B., Hammi, K. M., Trigui, I., Houissa, H., Mliki, A. & Hassouna, M. (2018). In vitro antifungal and anti-ochratoxigenic activities of Aloe vera gel against Aspergillus carbonarius isolated from grapes. Industrial Crops and Products, 123, 416-423. https://doi.org/10.1016/j.indcrop.2018.07.023
• Erdem, İ., Doğan, M., Karaali, R., Ardinç, E., & Elbasan Omar, Ş. (2018). İnvaziv Aspergilloz Tedavisi. Namık Kemal Tıp Dergisi, 6(2), 64–82. https://cms.galenos.com.tr/Uploads/Article_40406 /nkmj-6-64-En.pdf
• Hua, H., Xing, F., Selvaraj, J. N., Wang, Y., Zhao, Y., Zhou, L., Liu, X. & Liu, Y. (2014). Inhibitory effect of essential oils on Aspergillus ochraceus growth and ochratoxin A production. PloS One, 9(9), e108285. https://doi.org/10.1371/journal.pone.0108285
• IARC. (1993). International Agency for Research on Cancer, The evaluation of carcinogenic risk to human. (IARC monograph N 56), Lyon France, vol. 56, pp. 257-263.
• Kalagatur, N. K., Gurunathan, S., Kamasani, J. R., Gunti, L., Kadirvelu, K., Mohan, C. D., Rangappa, S., Prasad, R., Almeida, F., Mudili, V., & Siddaiah, C. (2020). Inhibitory effect of C. zeylanicum, C. longa, O. basilicum, Z. officinale, and C. martini essential oils on growth and ochratoxin A content of A. ochraceous and P. verrucosum in maize grains. Biotechnology Reports, 27, e00490. https://doi.org/10.1016/j.btre.2020.e00490
• Kapetanakou, A. E., Nestora, S., Evageliou, V., & Skandamis, P. N. (2019). Sodium alginate–cinnamon essential oil coated apples and pears: Variability of Aspergillus carbonarius growth and ochratoxin A production. Food Research International, 119, 876-885. https://doi.org/10.1016/j.foodres.2018.10.072
• Kostik, V., Gjorgjeska, B., & Petkovska, S. (2015). Mentha L. essential oils composition and in vitro antifungal activity. IOSR Journal of Pharmacy, 5(7), 1-7. http://www.iosrphr.org/pages /volume5-issue7.html
• Laaziz, A., El Hammoudi, Y., Qjidaa, S., Hajjaji, A., Hajjaj, H., Haesaert, G., & Bouseta, A. (2022). Activity of essential oils from Syzygium aromaticum and Rosmarinus officinalis against growth and ochratoxin A production by Aspergillus tubingensis and Aspergillus luchuensis from Moroccan grapes. Phytopathologia Mediterranea, 61(2), 299-310. https://doi.org/10.36253/phyto-12841
• Moghaddam, M., & Mehdizadeh, L. (2020). Chemical composition and antifungal activity of essential oil of Thymus vulgaris grown in Iran against some plant pathogenic fungi. Journal of Essential Oil Bearing Plants, 23(5), 1072-1083. https://doi.org/10.1080/0972060X.2020.1843547
• Moghaddam, M., Pourbaige, M., Tabar, H. K., Farhadi, N., & Hosseini, S. M. A. (2013). Composition and antifungal activity of peppermint (Mentha piperita) essential oil from Iran. Journal of Essential Oil Bearing Plants, 16(4), 506-512. https://doi.org/10.1080/0972060X.2013.813265
• Mseddi, K., Alimi, F., Noumi, E., Veettil, V. N., Deshpande, S., Adnan, M., Hamdi, A., Elkahoui, S., Alghamdi, A., Kadri, A., Patel, M., Snoussi, M., (2020). Thymus musilii Velen. as a promising source of potent bioactive compounds with its pharmacological properties: In vitro and in silico analysis. Arabian Journal of Chemistry, 13(8), 6782-6801. https://doi.org/10.1016 /j.arabjc.2020.06.032
• National Committee for Clinical Laboratory Standards. (2008). Reference method for broth dilution antifungal susceptibility testing of filamentous fungi; Approved Standard-Second Edition (NCCLS Standard No. M38-A2). https://clsi.org/standards/products/microbiology/ documents/m44/
• National Committee for Clinical Laboratory Standards. (2004). Method for Antifungal Disk Diffusion Susceptibility Testing of Yeasts; Approved Guideline. (NCCLS Standard No: M44-A). https://clsi.org/standards/products/microbiology/documents/m44/
• Navale, V., Vamkudoth, K. R., Ajmera, S., & Dhuri, V. (2021). Aspergillus derived mycotoxins in food and the environment: Prevalence, detection, and toxicity. Toxicology Reports, 8, 1008-1030. https://doi.org/10.1016/j.toxrep.2021.04.013
• Nerilo, S. B., Romoli, J. C. Z., Nakasugi, L. P., Zampieri, N. S., Mossini, S. A. G., Rocha, G. H. O., Micotti da Gloria, E., Alves de Abreu Filh, B., & Machinski Jr, M. (2020). Antifungal activity and inhibition of aflatoxins production by Zingiber officinale Roscoe essential oil against Aspergillus flavus in stored maize grains. Ciência Rural, 50, 1-10. https://doi.org/10.1590/0103-8478cr20190779
• Nurtjahja, K., Hastuti, L., Purnamasari, N., & Silitonga, G. N. (2022). Fungal Contamination and Toxigenicity of Aspergillus flavus on Postharvest Cacao Beans in Northern Sumatera, Indonesia. Yuzuncu Yıl University Journal of Agricultural Sciences, 32(3), 448-454. https://doi.org/10.29133/yyutbd.1071092
• Öncel, S., & Keçeli, S. A. (2018). Flukonazol. Mantar Dergisi, 9(1), 67-75. https://doi.org/10.30708/mantar.371030
• Özcan Ateş, G. & Kanbur, S. (2023). Evaluation of In-vitro Anticandidal Activity of 99 Different Commercial Plant Extract, Fixed and Essential Oils against Vaginal Candida albicans Isolates. Kahramanmaraş Sütçü İmam Üniversitesi Fen ve Mühendislik Dergisi, 26(5), 1034-1047. https://doi.org/10.18016/ksutarimdoga.vi.1211862
• Özcan Ateş, G. & Zorba, N. N. D. (2020). Determination of mycobiota and microbial loads of grapes grown in Bozcaada, Turkey. The Journal of Microbiology, Biotechnology and Food Sciences, 9(5), 899. https://doi.org/10.15414/jmbfs.2020.9.5.899-906
• Özcan Ateş, G. (2023). Antifungal activity of Eugenia caryophyllata, Cinnamomum sp., Mentha piperita, and Thymus vulgaris essential oils against Aspergillus niger. Anatolian Journal of Botany, 7(2), 135-139. https://doi.org/10.30616/ajb.1337945
• Özcan Ateş, G., Zorba, N. N. D., & Şen, B. (2024). Biodiversity of ochratoxigenic Aspergillus species isolated from çavuş and karalahna grapes in Bozcaada, Türkiye. Anatolian Journal of Botany, 8(1), 39-45. https://doi.org/10.30616/ajb.1395701
• Pantelides, I. S., Aristeidou, E., Lazari, M., Tsolakidou, M. D., Tsaltas, D., Christofidou, M., Kafouris, D., Christou, E., & Ioannou, N. (2017). Biodiversity and ochratoxin A profile of Aspergillus section Nigri populations isolated from wine grapes in Cyprus vineyards. Food Microbiology, 67, 106-115. https://doi.org/10.1016/j.fm.2017.06.010
• Pócsi, I., Giacometti, F., Ambrus, Á., & Logrieco, A. F. (2020). Aspergillus-derived mycotoxins in the feed and food chain. Frontiers in Microbiology, 11, 606108. https://doi.org/10.3389/ fmicb.2020.606108
• Ráduly, Z., Szabó, L., Madar, A., Pócsi, I., & Csernoch, L. (2020). Toxicological and medical aspects of Aspergillus-derived mycotoxins entering the feed and food chain. Frontiers in Microbiology, 10, 2908. https://doi.org/10.3389/fmicb.2019.02908
• Rodrigues, M. P., Astoreca, A. L., Oliveira, Á. A. D., Salvato, L. A., Biscoto, G. L., Keller, L. A. M., Rosa, C. A. .R., Cavaglieri, L. R., Azevedo, M. I., & Keller, K. M. (2019). In vitro activity of neem (Azadirachta indica) oil on growth and ochratoxin A production by Aspergillus carbonarius Isolates. Toxins, 11(10), 579. https://doi.org/10.3390/toxins11100579
• Satyal, P., Murray, B. L., McFeeters, R. L., & Setzer, W. N. (2016). Essential oil characterization of Thymus vulgaris from various geographical locations. Foods, 5(4), 70. https://doi.org/10.3390/ foods5040070
• Snoussi, M., Noumi, E., Punchappady-Devasya, R., Trabelsi, N., Kanekar, S., Nazzaro, F., Fratianni, F., Flamini, G., De Feo, V., Al-Sieni, A. (2018). Antioxidant properties and anti-quorum sensing potential of Carum copticum essential oil and phenolics against Chromobacterium violaceum. Journal of Food Science and Technology, 55(8), 2824-2832. https://doi.org/10.1007/s13197-018-3219-6
• Thippeswamy, S., Mohana, D. C., Abhishek, R. U., & Manjunath, K. (2014). Inhibitory activity of plant extracts on aflatoxin B1 biosynthesis by Aspergillus flavus. Journal of Agricultural Science and Technology, 16(5), 1123-1132. http://jast.modares.ac.ir/article-23-9949-en.html