Antifungal effects of some essential oils on selected allergenic fungi in vitro
Ewa Dorota Zalewska
Department of Vegetable and Herb Crops, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Lublin, Polandhttps://orcid.org/0000-0001-7445-9808
Grażyna Zawiślak
Department of Vegetable and Herb Crops, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Lublin, Polandhttps://orcid.org/0000-0002-4332-8394
Rafał Papliński
Department of Vegetable and Herb Crops, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Lublin, Polandhttps://orcid.org/0000-0002-3579-5785
Magdalena Walasek-Janusz
Department of Vegetable and Herb Crops, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Lublin, Polandhttps://orcid.org/0000-0002-7085-2212
Robert Gruszecki
Department of Vegetable and Herb Crops, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Lublin, Polandhttps://orcid.org/0000-0001-7108-1854
Abstract
The aim of the study was to determine the effect of four different essential oils on the sensitivity of allergenic fungi i.e. Alternaria alternata, Botrytis cinerea and Cladosporium cladosporioides. The studied fungi were isolated from infected fennel. The tested oils were added to Potato Dextrose Agar medium at the concentrations of 0.1 mg/mL, 0.25 mg/mL and 0.5 mg/mL. The activity of the oils on the inhibition of the linear growth of mycelium was evaluated by measuring of fungal colonies, while the fungistatic activity was evaluated on the basis of the percentage growth inhibition of fungal colony and calculated according to Abbot’s formula. The sensitivity of the tested isolates of fungi was variable and depended on the type and concentration of the studied essential oils. The most effective antifungal effect on all tested fungi was in essential oil of oregano even at the concentration of 0.1 mg/mL, while the weakest effect was in essential oil of grapefruit at all studied concentrations. Moreover, oregano essential oil caused degradation and decay of mycelium and spores. Essential oils are potential and promising antifungal agents used as bio fungicides in plant protection and indoor air disinfection. Therefore, further in vivo studies should be carried out.
Keywords:
Alternaria alternata, Cladosporium cladosporioides, Botrytis cinerea, essential oil, antifungal properties of essential oilsReferences
Abbas, N.B., Armin, S., Mahdieh, D., Ramin, N., Shahrokh, N., Rounak B. (2021). Pollution characteristics and noncarcinogenic risk assessment of fungal bioaerosol in different processing units of waste paper and cardboard recycling factory. Toxin Rev., 40(4), 752–763, https://doi.org/10.1080/15569543.2020.1769135 DOI: https://doi.org/10.1080/15569543.2020.1769135
Abd-El-Gawad, A.M., Elshamy, A.I., Al-Rowaily, S.L., El-Amier, Y.A. (2019). Habitat affects the chemical profile, allelopathy, and antioxidant properties of essential oils and phenolic enriched extracts of the invasive plant Heliotropium curassavicum. Plants, 8(11), 482. https://doi.org/10.3390/plants8110482 DOI: https://doi.org/10.3390/plants8110482
Abers, M., Schroeder, S., Goelz, L., Sulser, A., St. Rose, T., Puchalski, K., Langland, J. (2021). Antimicrobial activity of the volatile substances from essential oils. BMC Complement. Med. Ther., 21, 1–14. https://doi.org/10.1186/s12906-021-03285-3 DOI: https://doi.org/10.1186/s12906-021-03285-3
Alonso-Gato, M., Astray, G., Mejuto, J.C., Simal-Gandara, J. (2021). Essential oils as antimicrobials in crop protection. Antibiotics, 10(1), 34. https://doi.org/10.3390/antibiotics10010034 DOI: https://doi.org/10.3390/antibiotics10010034
Assaeed, A., Elshamy, A., El Gendy, A.E.-N., Dar, B., Al-Rowaily, S., Abd El-Gawad, A. (2020). Sesquiterpenes-rich essential oil from above ground parts of Pulicaria somalensis exhibited antioxidant activity and allelopathy effect on weeds. Agronomy, 10(3), 399. https://doi.org/10.3390/agronomy10030399 DOI: https://doi.org/10.3390/agronomy10030399
Azizi, A., Yan, F., Honermeier, B. (2009). Herbage yield, essential oil content and composition of three oregano (Origanum vulgare L.) populations as affected by soil moisture regimes and nitrogen supply. Ind. Crops Prod., 29(2–3), 554–561. https://doi.org/10.1016/j.indcrop.2008.11.001 DOI: https://doi.org/10.1016/j.indcrop.2008.11.001
Babar, A., Naser, A.Al-W., Saiba, S., Aftab, A., Shah, A.K., Firoz, A. (2015). Essential oils used in aromatherapy: a systemic review. Asian Pac. J. Trop. Biomed., 5(8), 601–611. https://doi.org/10.1016/j.apjtb.2015.05.007 DOI: https://doi.org/10.1016/j.apjtb.2015.05.007
Badawy, M.E., Abdelgaleil, S.A. (2014). Composition and antimicrobial activity of essential oils isolated from Egyptian plants against plant pathogenic bacteria and fungi. Ind. Crops Prod., 52, 776–782. https://doi.org/10.1016/j.indcrop.2013.12.003 DOI: https://doi.org/10.1016/j.indcrop.2013.12.003
Bakkali, F., Averbeck, S., Averbeck, D., Idaomar, M. (2008). Biological effects of essential oils – a review. Food Chem. Toxicol., 46(2), 446–475. https://doi.org/10.1016/j.fct.2007.09.106 DOI: https://doi.org/10.1016/j.fct.2007.09.106
Behnam, S., Farzaneh, M., Ahmadzadeh, M., Tehrani, A.S. (2006). Composition and antifungal activity of essential oils of Mentha piperita and Lavendula angustifolia on post-harvest phytopathogens. Commun. Agric. Appl. Biol. Sci., 71(3 Pt B), 1321–1326.
Bennike, N.H., Johansen, J.D. (2018). Aromatherapists. In: Kanerva’s occupational dermatology, John, S., Johansen, J., Rustemeyer, T., Elsner, P., Maibach, H. (eds). Springer, Cham, 1–4. DOI: https://doi.org/10.1007/978-3-319-40221-5_118-2
Bhalla, Y., Gupta, V.K., Jaitak, V. (2013). Anticancer activity of essential oils: a review. J. Sci. Food Agric., 93(15), 3643–3653. https://doi.org/10.1002/jsfa.6267 DOI: https://doi.org/10.1002/jsfa.6267
Burgieł, Z.J., Smagłowski, M. (2008). Fungistic properties of tea tree oil. Probl. J. Agric. Sci., 529, 13–18.
De Hoog, G.S., Guarro, J., Gené, J., Figueras, M.J. (2000). Atlas of clinical fungi, 2nd ed. Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands.
Elgamal, A.M., Ahmed, R.F., Abd-ElGawad, A.M., El Gendy, A.E.-N.G., Elshamy, A.I., Nassar, M.I. (2021). Chemical profiles, anticancer, and anti-aging activities of essential oils of Pluchea dioscoridis (L.) DC. and Erigeron bonariensis L. plants, 10(4), 667. https://doi.org/10.3390/plants10040667 DOI: https://doi.org/10.3390/plants10040667
Elshamy, A.I., Ammar, N.M., Hassan, H.A., Al-Rowaily, S.L., Raga, T.R., El Gendy, A., Abd El-Gawad, A.M. (2020). Essential oil and its nanoemulsion of Araucaria heterophylla resin: chemical characterization, anti-inflammatory, and antipyretic activities. Ind. Crop. Prod., 148, 112272. https://doi.org/10.1016/j.indcrop.2020.112272 DOI: https://doi.org/10.1016/j.indcrop.2020.112272
Feng, W., Zheng, X. (2007). Essential oils to control Alternaria alternata in vitro and in vivo. Food control, 18(9), 1126–1130. https://doi.org/10.1016/j.foodcont.2006.05.017 DOI: https://doi.org/10.1016/j.foodcont.2006.05.017
Fengfeng, W., Yamei, J., Xueming, X., Na, Y. (2017). Eletrofluidic pretreatment for enhancing essential oil extraction from citrus fruit peel waste. J. Clean. Prod., 159, 85–94. https://doi.org/10.1016/J.JCLEPRO.2017.05.010 DOI: https://doi.org/10.1016/j.jclepro.2017.05.010
Fidanza, M.R., Caneva, G. (2019). Natural biocides for the conservation of stone cultural heritage: a review. J. Cult. Herit., 38, 271–286. https://doi.org/10.1016/J.JCLEPRO.2017.05.01010.1016/j.culher.2019.01.005 DOI: https://doi.org/10.1016/j.culher.2019.01.005
Garbusińska, A., Mertas, A., Król, W. (2010). Przegląd badań in vitro oceniających aktywność przeciwdrobnoustrojową olejku z drzewa herbacianego (Tea Tree Oil). Cz. I [The antimicrobial activity of tea tree oil in the research in vitro. Part I]. Borgis – Post. Fitoter., 2, 85–96.
Garbusińska, A., Mertas, A., Szliszka, E., Król, W. (2011). Aktywność przeciwdrobnoustrojowa olejku z drzewa herbacianego (Tea Tree Oil) w badaniach in vitro. Cz. II [The antimicrobial activity of tea tree oil in the research in vitro. Part II], Borgis – Post Fitoter., 3, 175–184.
Góra, J., Lis, A. (2019). Najcenniejsze olejki eteryczne. Cz. 1 [The most valuable essential oils. Part 1]. Wydawnictwo Politechniki Łódzkiej [TUL Publishing House], 68–72, 165–170 [in Polish].
Gwiazdowski, R., Gwiazdowska, D., Marchwińska, K., Juś, K., Szutowska, J., Bednarek-Bartsch, A., Danielewicz, B. (2018). Właściwości fungistatyczne olejków eterycznych wobec wybranych patogenów rzepaku [Fungistatic activity of essential oils towards selected oilseed rape pathogens]. Progress Plant Protect., 58(4), 300–305 [in Polish]. https://doi.org/10.14199/ppp-2018-042 DOI: https://doi.org/10.14199/ppp-2018-042
Halberstein, R. (2005). Medicinal plants: historical and cross-cultural usage patterns. Ann. Epidemiol., 15(9), 686–699. https://doi.org/10.1016/j.annepidem.2005.02.004 DOI: https://doi.org/10.1016/j.annepidem.2005.02.004
Hou, H., Zhang, X., Zhao, T., Zhou, L. (2020). Effects of Origanum vulgare essential oil and its two main components, carvacrol and thymol, on the plant pathogen Botrytis cinerea. Peer J., 8, e9626. https://doi.org/10.7717/peerj.9626 DOI: https://doi.org/10.7717/peerj.9626
Jurgensen, C.W., Madsen, A. (2009). Exposure to the airborne mould Botrytis and its health effects. Ann. Agric. Environ. Med., 16(2), 183–196.
Kaur, N., Bains, A., Kaushik, R., Dhull, S.B., Melinda, F., Chawla, P. (2021). A review on antifungal efficiency of plant extracts entrenched polysaccharide-based nanohydrogels. Nutrients, 13(6), 2055. https://doi.org/10.3390/nu13062055 DOI: https://doi.org/10.3390/nu13062055
Kilic, M., Altunoglu, M.K., Akdogan, G.E., Akpınar, S., Taskın, E., Erkal, A.H. (2020). Airborne fungal spore relationships with meteorological parameters and skin prick test results in Elazig, Turkey. J. Environ. Health Sci. Engineer, 18, 1271–1280. https://doi.org/10.1007/s40201-020-00545-1 DOI: https://doi.org/10.1007/s40201-020-00545-1
Lis, A. (2019). Najcenniejsze olejki eteryczne. Cz. 2 [The most valuable essential oils. Part 2]. Wydawnictwo Politechniki Łódzkiej [TUL Publishing House], 69–80.
Machowicz-Stefaniak, Z., Zalewska, E. (2011). Occurrence of Colletotrichum dematium on selected herbs species and preparations inhibiting pathogen’s growth and development in vitro. Ecol. Chem. Eng., 18(4), 465–478.
Malik, A., Najda, A., Bains, A., Nurzyńska-Wierdak, R., Chawła, P. (2021). Characterization of Citrusnobilis peel methanolic extract for antioxidant, antimicrobial, and anti-inflammatory activity. Molecules, 26(14), 4310. https://doi.org/10.3390/molecules26144310 DOI: https://doi.org/10.3390/molecules26144310
Mendes de Toledo, C.E., Santos, P.R., Palazzo de Mello, J.C., Dias Filho, B.P., Nakamura, C.V., Ueda-Nakamura, T. (2015). Antifungal properties of crude extracts, fractions, and purified compounds from bark of Curatella americana L. (Dilleniaceae) against Candida species. Evid. Based Complement. Alternat. Med., 673962. https://doi.org/10.1155/2015/673962 DOI: https://doi.org/10.1155/2015/673962
Nazzaro, F., Fratianni, F., Coppola, R., Feo, V.D. (2017). Essential oils and antifungal activity. Pharmaceuticals, 10(4), 86. https://doi.org/10.3390/ph10040086 DOI: https://doi.org/10.3390/ph10040086
Özcan, M.M., Starovic, M., Aleksic, G., Figueredo, G., Juhaimi, F.A., Chalchat, J-C. (2018). Chemical composition and antifungal activity of lavender (Lavandula stoechas) oil. Nat. Prod. Commun. https://doi.org/10.1177/1934578X1801300728 DOI: https://doi.org/10.1177/1934578X1801300728
Palfi, M., Konjevoda, P., Vrandečić, K. (2019). Antifungal activity of essential oils on mycelial growth of Fusarium oxysporum and Bortytis cinerea. Emir. J. Food Agric., 31(7), 544–554. https://doi.org/10.9755/ejfa.2019.v31.i7.1972. DOI: https://doi.org/10.9755/ejfa.2019.v31.i7.1972
Patkowska, E., Krawiec, M. (2016). Yielding and healthiness of pea cv. ‘Sześciotygodniowy’ after applying biotechnical preparations. Acta Sci. Pol. Hortorum Cultus, 15(2), 143–156.
Peighami-Ashnaei, S., Farzaneh, M., Sharifi-Tehrani, A., Behboudi, K. (2009). Effect of essential oils in control of plant diseases. Commun. Agric. Appl. Biol. Sci., 74(3), 843–847.
Raveau, R., Fontaine, J., Lounès-Hadj Sahraoui, A. (2020). Essential oils as potential alternative biocontrol products against plant pathogens and weeds: a review. Foods, 9(3), 365. https://doi.org/10.3390/foods9030365 DOI: https://doi.org/10.3390/foods9030365
Sabariego, S., Bouso, V., Pérez-Badia, R. (2012). Comparative study of airborne Alternaria conidia levels in two cities in Castilla-La Mancha (central Spain), and correlations with weather-related variables. Ann. Agric. Environ. Med., 19(2), 227–232.
Salvatore, M.M., Nicoletti, R., Andolfi, A. (2022). Essential oils in citrus fruit ripening and postharvest quality. Horticulturae, 8(5), 396. https://doi.org/10.3390/horticulturae8050396 DOI: https://doi.org/10.3390/horticulturae8050396
Sapieha-Waszkiewicz, A., Marjańska-Cichoń, B., Miętkiewski, R. (2011). Effect of biopesticides on the growth and development of isolates of Botrytis cinerea Pers., in vitro obtained from raspberry plants. J. Plant Protect. Res., 51(2), 151–156. https://doi.org/10.2478/v10045-011-0026-8 DOI: https://doi.org/10.2478/v10045-011-0026-8
Simon-Nobbe, B., Denk, U., Pöll, V., Rid, R., Breitenbach, M. (2008). The spectrum of fungal allergy. Int. Arch. Allergy Immunol., 145(1), 58–86. https://doi.org/10.1159/000107578 DOI: https://doi.org/10.1159/000107578
Singh, K. (2019). Keeping with tradition: essential oil history, use and production: a review. Cosmet. Toilet., 134(7), 61–70.
Sio, Y.Y., Pang, S.L., Say, YH., Teh, K.F., Wong, Y.R., Shah, S.M.R., Reginald, K., Chew F.T. (2021). Sensitization to airborne fungal allergens associates with asthma and allergic rhinitis presentation and severity in the Singaporean/Malaysian population. Mycopathologia, 186, 583–588. https://doi.org/10.1007/s11046-021-00532-6 DOI: https://doi.org/10.1007/s11046-021-00532-6
Skyberg, K., Skulberg, K.R., Eduard, W. (2003). Symptoms prevalence among office employees and associations to building characteristics. Indoor Air, 13(3), 246–252. https://doi.org/10.1034/j.1600-0668.2003.00190.x DOI: https://doi.org/10.1034/j.1600-0668.2003.00190.x
Soares-Castro, P., Soares, F., Santos, P.M. (2021). Current advances in the bacterial toolbox for the biotechnological production of monoterpene-based aroma compounds. Molecules, 26(1), 91. https://doi.org/10.3390/molecules26010091 DOI: https://doi.org/10.3390/molecules26010091
Soylu, E.M., Kurt, S., Soylu, S. (2010). In vitro and in vivo antifungal activities of the essential oils of various plants against tomato grey mold disease agent Botrytis cinerea. Int. J. Food Microbiol., 143(3), 183–189, https://doi.org/10.1016/j.ijfoodmicro.2010.08.015 DOI: https://doi.org/10.1016/j.ijfoodmicro.2010.08.015
Soylu, S., Yigitbas, H., Soylu, E.M., Kurt, S. (2007). Effects of essential oils from oregano and fennel on Sclerotinia sclerotiorum. J. Appl. Microbiol., 103(4), 1021–1030. https://doi.org/10.1111/j.1365-2672.2007.03310.x DOI: https://doi.org/10.1111/j.1365-2672.2007.03310.x
Tongnuanchan, P., Benjakul, S. (2014). Essential oils: extraction, bioactivities, and their uses for food preservation. J. Food Sci., 79(7), 1231–1249. https://doi.org/10.1111/1750-3841.12492 DOI: https://doi.org/10.1111/1750-3841.12492
Turek C., Stintzing, C. (2013). Stability of essential oils: a review. Compr. Rev. Food Sci. Food Saf., 12(1), 40–53. https://doi.org/10.1111/1541-4337.12006 DOI: https://doi.org/10.1111/1541-4337.12006
Wang, K., Jiang, S., Yang, Y., Fan, L., Su, F., Ye, M. (2019). Synthesis and antifungal activity of carvacrol and thymol esters with heteroaromatic carboxylic acids. Nat. Prod. Res., 33(13), 1924–1930. https://doi.org/10.1080/14786419.2018.1480618 DOI: https://doi.org/10.1080/14786419.2018.1480618
Weryszko-Chmielewska, E., Kasprzyk, I., Nowak, M., Sulborska, A., Kaczmarek, J., Szymanska, A., Haratym, W., Gilski, M., Jedryczka, M. (2018). Health hazards related to conidia of Cladosporium – biological air pollutants in Poland, central Europe. J. Environ. Sci., 65, 271–281. https://doi.org/10.1016/j.jes.2017.02.018 DOI: https://doi.org/10.1016/j.jes.2017.02.018
Whiley, H., Gaskin, S., Schroder, T., Ross, K. (2018). Antifungal properties of essential oils for improvement of indoor air quality: a review. Rev. Environ. Health., 33(1), 63–76. https://doi.org/10.1515/reveh-2017-0023 DOI: https://doi.org/10.1515/reveh-2017-0023
Yu, D., Wang, J., Shao, X., Xu, F., Wang, H. (2015). Antifungal modes of action of tea tree oil and its two characteristic components against Botrytis cinerea. J. Appl. Microbiol., 119(5), 1253–1262. https://doi.org/10.1111/jam.12939 DOI: https://doi.org/10.1111/jam.12939
Zabka, M., Pavela, R., Prokinova, E. (2014). Antifungal activity and chemical composition of twenty essential oils against significant indoor and outdoor toxigenic and aeroallergenic fungi. Chemosphere, 112, 443–448. https://doi.org/10.1016/j.chemosphere.2014.05.014 DOI: https://doi.org/10.1016/j.chemosphere.2014.05.014
Zhou, H.E., Tao, N.G., Jia, L. (2014). Antifungal activity of citral, octanal and α-terpineol against Geotrichum citri-aurantii. Food Control, 37, 277–283. https://doi.org/10.1016/j.foodcont.2013.09.057 DOI: https://doi.org/10.1016/j.foodcont.2013.09.057
Department of Vegetable and Herb Crops, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Lublin, Poland https://orcid.org/0000-0001-7445-9808
Department of Vegetable and Herb Crops, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Lublin, Poland https://orcid.org/0000-0002-4332-8394
Department of Vegetable and Herb Crops, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Lublin, Poland https://orcid.org/0000-0002-3579-5785
Department of Vegetable and Herb Crops, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Lublin, Poland https://orcid.org/0000-0002-7085-2212
Department of Vegetable and Herb Crops, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Lublin, Poland https://orcid.org/0000-0001-7108-1854
License

This work is licensed under a Creative Commons Attribution 4.0 International License.
Articles are made available under the conditions CC BY 4.0 (until 2020 under the conditions CC BY-NC-ND 4.0).
Submission of the paper implies that it has not been published previously, that it is not under consideration for publication elsewhere.
The author signs a statement of the originality of the work, the contribution of individuals, and source of funding.