Comprehensive Evaluation of Antifungal Activity of Argania spinosa (L.) Skeels kernels of the Hot and Cold Extraction and the Effect of Solvents Varying Polarities and the Heat Treatment on Yield and Activity Variance

https://doi.org/10.22146/ifnp.79710

Aziza Lfitat(1*), Imad Ed-dahmani(2), Fatima Zohra Bousraf(3), Abdelhaq Belhaj(4), Tarik Ainane(5), Mustapha Taleb(6), Abdelkader Gourch(7), Abdelfattah Abdellaoui(8)

(1) Laboratory of Engineering, Organometallic, Molecular Materials and Environment (LIMOME), Department of Chemistry, Faculty of Sciences Sidi Mohamed Ben Abdellah University.
(2) Laboratory of Engineering, Organometallic, Molecular Materials and Environment (LIMOME), Department of Chemistry, Faculty of Sciences, Sidi Mohamed Ben Abdellah University, P.O. Box 1796 (Atlas), 30000 Fez
(3) Laboratory of Engineering, Organometallic, Molecular Materials and Environment (LIMOME), Department of Chemistry, Faculty of Sciences, Sidi Mohamed Ben Abdellah University, P.O. Box 1796 (Atlas), 30000 Fez
(4) Laboratory of Environment, Ecology, and Health, Department of Biology, Faculty of Sciences, Moulay Ismail University, B.P. 11201 Zitoune, Meknes
(5) Superior School of Technology, University of Sultan Moulay Slimane, B. P. 170, 54000 Khenifra
(6) Laboratory of Engineering, Organometallic, Molecular Materials and Environment (LIMOME), Department of Chemistry, Faculty of Sciences, Sidi Mohamed Ben Abdellah University, P.O. Box 1796 (Atlas), 30000 Fez
(7) Laboratory of Engineering, Organometallic, Molecular Materials and Environment (LIMOME), Department of Chemistry, Faculty of Sciences, Sidi Mohamed Ben Abdellah University, P.O. Box 1796 (Atlas), 30000 Fez
(8) Laboratory of Engineering, Organometallic, Molecular Materials and Environment (LIMOME), Department of Chemistry, Faculty of Sciences, Sidi Mohamed Ben Abdellah University, P.O. Box 1796 (Atlas), 30000 Fez
(*) Corresponding Author

Abstract


A comparative antifungal efficacy study of argan kernels was performed using different solvent fractions obtained by the two extraction methods: cold extraction by maceration at room temperature (1) and hot extraction by Soxhlet apparatus (2). Results demonstrated that the two extraction methods induce different yields among each solvent used. Maceration promoted the maximum contents of crude extract in hexane (42.15%), diethyl ether (2.59%), dichloromethane (4.22%), and ethyl acetate (2.52%). Whereas the hot extraction yielded higher extractives in the case of methanol (22.97%) and water (5.88%) compared to cold extraction. The MIC values of the fractionated extracts obtained by maceration were in the range of 0.051 ± 0.002 and 0.223 ± 0.005 g/ml, whilst they were in the range of 0.101 ± 0.002 and 0.286 ± 0.005 g/ml for the Soxhlet extracts. According to total activity (TA) interpretation, dichloromethane was the most effective solvent to extract active antifungal components, revealing the strongest ability to suppress the growth of fungi at much lower MIC values (0.051 ± 0.002 to 0.156 ± 0.005 g/ml) than the rest of fractions. The effect of heating resulted in an increase of the MICs values of the Soxhlet extracts from 10 to 25 times higher than macerated ones, resulting in lower antifungal activity. 


Keywords


argan kernel; Aspergillus fumigatus; Aspergillus niger; Plasmodium brasilianum; Fusarium dimerium

Full Text:

PDF


References

Adam, O.A.O., Abadi, R.S.M. and Ayoub, S.M.H. (2019). The effect of extraction method and solvents on yield and antioxidant activity of certain Sudanese medicinal plant extracts. The Journal of Phytopharmacology. 8(5):248-252.

Ahansal, L., Ben Sassi, A., Martini, A., Vaughan-Martini, A., Walker, G. and Boussaid, A. (2008). Biodiversity of yeasts isolated from the indigenous forest of argan (Argania spinosa (L.) Skeels) in Morocco. World Journal of Microbiology and Biotechnology, 24(6), 777–782.

Ait Aabd, N., Bouharroud, R., Tahiri, A., Wifaya, A., Mimouni, A. and El Mousadik, A. (2019). Genetic diversity and breeding of argan tree (Argania spinosa L. Skeels). In “Advances in plant breeding strategies: nut and beverage crops”. ed. J.M. Al-Khayri, S.M. Jain, and D.V. Johnson, pp. 31-56. Springer Nature, Cham, Switzerland.

Alvarenga, D.A., Pina-Costa, A., Bianco, C., Moreira, S.B., Brasil, P., Pissinatti, A., Daniel-Ribeiro, C.T. and Brito, C.F. (2017). New potential Plasmodium brasilianum hosts: tamarin and marmoset monkeys (family Callitrichidae). Malaria Journal, 16(1), 1-7.

Al-Zubaidi, S., Al-Ayafi, A. and Abdelkader, H. (2019). Biosynthesis, characterization and antifungal activity of silver nanoparticles by Aspergillus niger isolate. Journal of Nanotechnology Research, 1(1), 23-36.

Andersen, M.R., Salazar, M.P., Schaap, P.J., van de Vondervoort, P.J., Culley, D., Thykaer, J., Frisvad, J.C., Nielsen, K.F., Albang, R., Albermann, K., Berka, R.M., Braus, G.H., Braus-Stromeyer, S.A., Corrochano, L.M., Dai, Z., van Dijck, P.W., Hofmann, G., Lasure, L.L., Magnuson, J.K., Menke, H., Meijer, M., Meijer, S.L., Nielsen, J.B., Nielsen, M.L., van Ooyen, A.J., Pel, H.J., Poulsen, L., Samson, R.A., Stam, H., Tsang, A., van den Brink, J.M., Atkins, A., Aerts, A., Shapiro, H., Pangilinan, J., Salamov, A., Lou, Y., Lindquist, E., Lucas, S., Grimwood, J., Grigoriev, I.V., Kubicek, C.P., Martinez, D., van Peij, N.N., Roubos, J.A., Nielsen, J. and Baker, S.E. 2011. Comparative genomics of citric-acid-producing Aspergillus niger ATCC 1015 versus enzyme-producing CBS 513.88. Genome Research, 21(6), 885-897.

Atifi, H., Jadouali, S.M., Laknifli, A., Bouzoubaâ, Z., Mamouni, R., Faouzi, A. and Achemchem, F. 2019. Effect of ripening degree of argane fruit on the phenolic composition and antioxidant activity of the fruit pulp, kernel, and oil. Moroccan Journal of Chemistry, 7(2), 7-2.

Baig, M.W., Ahmed, M., Akhtar, N., Okla, M.K., Nasir, B., Haq, I.U., Al-Ghamdi, J., Al-Qahtani, W.H. and AbdElgawad, H. (2021). Caralluma tuberculata NE Br manifests extraction medium-reliant disparity in phytochemical and pharmacological analysis. Molecules, 26(24), 7530.

Bani-Aameur, F. and Ferradous, A. 2001. Fruits and stone variability in three argan (Argania spinosa (L.) Skeels) populations. Forest Genetics, 8(1):39-43.

Barbara, D.A. (2017). M38 Reference method for broth dilution antifungal susceptibility testing of filamentous fungi. CLSI.

Barber, A.E., Riedel, J., Sae-Ong, T., Kang, K., Brabetz, W., Panagiotou, G., Deising, H.B. and Kurzai, O. 2020. Effects of agricultural fungicide use on Aspergillus fumigatus abundance, antifungal susceptibility, and population structure. MBio. 11(6):e02213-20.

Bongomin, F., Gago, S., Oladele, R.O. and Denning, D.W. (2017). Global and multi-national prevalence of fungal diseases—estimate precision. Journal of Fungi, 3(4), 57.

Brown, G. D., Denning, D. W., Gow, N. A., Levitz, S. M., Netea, M. G. and White, T. C. (2012). Hidden killers: human fungal infections. Science Translational Medicine, 4(165), 165rv13. https://doi.org/10.1126/scitranslmed.3004404

Cairns, T. C., Barthel, L. and Meyer, V. (2021). Something old, something new: challenges and developments in Aspergillus niger biotechnology. Essays in Biochemistry 65(2), 213–224.

Cairns, T. C., Nai, C. and Meyer, V. (2018). How a fungus shapes biotechnology: 100 years of Aspergillus niger research. Fungal Biology and Biotechnology, 5(1), 1–14.

Charrouf, Z. and Guillaume, D. (2014). Argan oil, the 35‐years‐of‐research product. European Journal of Lipid Science and Technology, 116(10), 1316–1321.

Chhetri, H. P., Yogol, N. S., Sherchan, J., Anupa, K. C., Mansoor, S. and Thapa, P. 2008. Phytochemical and antimicrobial evaluations of some medicinal plants of Nepal. Kathmandu University Journal of Science, Engineering and Technology, 4(1), 49-54.

Choi, M. S., Kim, J. K., Kim, D. H. and Yoo, H. H. (2019). Effects of gut microbiota on the bioavailability of bioactive compounds from ginkgo leaf extracts. Metabolites, 9(7), 132.

Christensen, M. and Tuthill, D.E. (1986). Aspergillus: An overview. In “Advances in penicillium and aspergillus systematics”. ed. R.A. Samson, and J.I. Pitt, pp. 195-209. NATO ASI Series, Springer, Boston, MA.

Deaguero, I.G., Huda, M.N., Rodriguez, V., Zicari, J., Al-Hilal, T.A., Badruddoza, A.Z.M. and Nurunnabi, M. (2020). Nano-vesicle-based anti-fungal formulation shows higher stability, skin diffusion, biosafety, and anti-fungal efficacy in vitro. Pharmaceutics. 12(6),516.

do Carmo, A., Costa, E., Marques, M., Quadrado, M. J. and Tomé, R. (2016). Fusarium dimerum species complex (Fusarium penzigii) keratitis after corneal trauma. Mycopathologia, 181(11), 879-884.

Eloff, J.N. (2004). Quantifying the bioactivity of the plant extracts during screening and bioassay-guided fractionation. Phytomedicine. 11(4), 370–371.

El Alaoui, N. (1999). Paysages, usages et voyages d'Argania spinosa (L.) Skeels (IXe-Xe siècles). Journal d'Agriculture Traditionnelle et de Botanique Appliquée, 41(2), 45-79.

El Monfalouti, H., Charrouf, Z., Belviso, S., Ghirardello, D., Scursatone, B., Guillaume, D., Denhez, C. and Zeppa, G. (2012). Analysis and antioxidant capacity of the phenolic compounds from argan fruit (Argania spinosa (L.) Skeels). European Journal of Lipid Science and Technology, 114(4), 446-452.

Escalante, A.A., Barrio, E. and Ayala, F.J. 1995. Evolutionary origin of human and primate malarias: evidence from the circumsporozoite protein gene. Molecular biology and Evolution. 12(4), 616-626.

Farahani, Z.K. (2021). The effect of extraction method (ultrasonic, maceration, and soxhlet) and solvent type on the extraction rate of phenolic compounds and extraction efficiency of Arctium lappa L. roots and Polygonum aviculare L. grass. Food & Health. 4(2): 28-34.

Favel, A., Steinmetz, M.D., Regli, P., Vidal-Ollivier, E., Elias, R. and Balansard, G. (1994). In vitro antifungal activity of triterpenoid saponins. Planta Medica. 60(01):50-53.

Fisher, M.C., Gurr, S.J., Cuomo, C.A., Blehert, D.S., Jin, H., Stukenbrock, E.H., Stajich, J.E., Kahmann, R., Boone, C., Denning, D.W., Gow, N.A.R., Klein, B.S., Kronstad, J.W., Sheppard, D.C., Taylor, J.W., Wright, G.D., Heitman, J., Casadevall, A. and Cowen, L.E. (2020). Threats posed by the fungal kingdom to humans, wildlife, and agriculture. MBio. 11(3), e00449-20.

Guillaume, D. and Charrouf, Z. (2005). Saponines et métabolites secondaires de l'arganier (Argania spinosa). Cahiers Agricultures, 14(6), 509-516.

Guillaume, D. and Charrouf, Z. (2011). Argan oil and other argan products: use in dermo cosmetology. European Journal of Lipid Science and Technology. 113(4):403-408.

Guimarães, L.O., Bajay, M.M., Wunderlich, G., Bueno, M.G., Röhe, F., Catão-Dias, J.L., Neves, A., Malafronte, R.S., Curado, I. and Kirchgatter, K. 2012. The genetic diversity of Plasmodium malariae and Plasmodium brasilianum from human, simian and mosquito hosts in Brazil. Acta Tropica, 124(1), 27-32.

Haldane, D.J. and Robart, E. (1990). A comparison of calcofluor white, potassium hydroxide, and culture for the laboratory diagnosis of superficial fungal infection. Diagnostic Microbiology and Infectious Disease, 13(4), 337-339.

Harhar, H., Gharby, S., Kartah, B., El Monfalouti, H., Guillaume, D. and Charrouf, Z. (2011). Influence of argan kernel roasting-time on virgin argan oil composition and oxidative stability. Plant Foods for Human Nutrition, 66(2), 163-168.

Hilali, M., Charrouf, Z., Aziz Soulhi, A.E., Hachimi, L. and Guillaume, D. (2005). Influence of origin and extraction method on argan oil physico-chemical characteristics and composition. Journal of Agricultural and Food Chemistry. 53(6), 2081-2087.

Jasuja, N. D., Sharma, S. K., Saxena, R., Choudhary, J., Sharma, R. and Joshi, S. C. (2013). Antibacterial, antioxidant, and phytochemical investigation of Thuja orientalis leaves. Journal of Medicinal Plants Research, 7(25), 1886-1893.

Karaalp, C., Yurtman, A. N. and Karabay Yavasoglu, N. U. (2009). Evaluation of antimicrobial properties of Achillea L. flower head extracts. Pharmaceutical Biology, 47(1), 86-91.

Khalid, S. N., Rizwan, N., Khan, Z. A., Najam, A., Khan, A. M., Almas, T., Khedro, T., Nagarajan, V. R., Alshamlan, A., Gronfula, A., Alshehri, R. and Alshehri, R. (2021). Fungal burn wound infection caused by Fusarium dimerum: a case series on a rare etiology. Annals of Medicine and Surgery. 70, 102848.

Khallouki, F., Younos, C., Soulimani, R., Oster, T., Charrouf, Z., Spiegelhalder, B., Bartsch, H. and Owen, R. W. (2003). Consumption of argan oil (Morocco) with its unique profile of fatty acids, tocopherols, squalene, sterols, and phenolic compounds should confer valuable cancer chemopreventive effects. European Journal of Cancer Prevention, 67-75.

Kharbach, M., Marmouzi, I., Kamal, R., Yu, H., Barra, I., Cherrah, Y., Alaoui, K., Vander Heyden, Y. and Bouklouze, A. (2021). Extra virgin Argan oils’ shelf-life monitoring and prediction based on chemical properties or FTIR fingerprints and chemometrics. Food Control. 121, 107607.

Koch, B. E., Hajdamowicz, N. H., Lagendijk, E., Ram, A. F. and Meijer, A. H. (2019). Aspergillus fumigatus establishes infection in zebrafish by germination of phagocytized conidia, while Aspergillus niger relies on extracellular germination. Scientific Reports. 9(1):1-13.

Kumari, M. and Singh, M. (2017). Bio-intensive Management of collar rot disease of groundnut (Arachis hypogea L.) caused by Aspergillus niger. International Journal of Chemical Studies. 5(4), 80–82.

Lalremruata, A., Magris, M., Vivas-Martínez, S., Koehler, M., Esen, M., Kempaiah, P., Jeyaraj, S., Perkins, D. J., Mordmüller, B. and Metzger, W. G. (2015). Natural infection of Plasmodium brasilianum in humans: man and monkey share quartan malaria parasites in the Venezuelan Amazon. EBioMedicine. 2(9), 1186-1192.

Lourenço-de-Oliveira, R. and Deane, L. M. (1995). Simian malaria at two sites in the Brazilian Amazon: I-the infection rates of Plasmodium brasilianum in non-human primates. Memórias do Instituto Oswaldo Cruz. 90, 331-339.

Mahlo, S.M., Chauke, H.R., McGaw, L. and Eloff, J. (2016). Antioxidant and antifungal activity of selected medicinal plant extracts against phytopathogenic fungi. African Journal of Traditional, Complementary and Alternative Medicines. 13(4), 216-222.

Matthäus, B., Guillaume, D., Gharby, S., Haddad, A., Harhar, H. and Charrouf, Z. (2010). Effect of processing on the quality of edible argan oil. Food Chemistry. 120(2), 426-432.

Masoko, P., Picard, J. and Eloff, J.N. (2005). Antifungal activities of six South African Terminalia species (Combretaceae). Journal of Ethnopharmacology, 99(2), 301-308.

Mechqoq, H., El Yaagoubi, M., El Hamdaoui, A., Momchilova, S., da Silva Almeida, J.R.G., Msanda, F. and El Aouad, N. 2021. Ethnobotany, phytochemistry and biological properties of argan tree (Argania spinosa (L.) Skeels) (Sapotaceae)-a review. Journal of Ethnopharmacology, 281, 114528.

Mert-Türk, F. (2006). Saponins versus plant fungal pathogens. Journal of Cell and Molecular Biology, 5, 13-17.

Metougui, M.L., Mokhtari, M., Maughan, P.J., Jellen, E.N. and Benlhabib, O. (2017). Morphological variability, heritability, and correlation studies within an argan tree population (Argania spinosa (L.) Skeels) preserved in situ. International Journal of Agriculture and Forestry, 7(2), 42-51.

Mostafa, A., Sudisha, J., El-Sayed, M., Ito, S.I., Ikeda, T., Yamauchi, N. and Shigyo, M. (2013). Aginoside saponin, a potent antifungal compound, and secondary metabolite analyses from Allium nigrum L. Phytochemistry Letters, 6(2), 274-280.

Ngamwonglumlert, L., Devahastin, S. and Chiewchan, N. (2017). Natural colorants: Pigment stability and extraction yield enhancement via utilization of appropriate pretreatment and extraction methods. Critical Reviews in Food Science and Nutrition. 57(15):3243-3259.

Nicoletti, G. and White, K. (2022). The anti-fungal activity of nitropropenyl benzodioxole (NPBD), a redox-thiol oxidant and tyrosine phosphatase inhibitor. Antibiotics, 11(9):1188.

Laxminarayan, R., Duse, A., Wattal, C., Zaidi, A. K., Wertheim, H. F., Sumpradit, N., Vlieghe, E., Levy-Hara, G., Gould, I. M., Goossens, H., Greko, C., So, A. D., Bigdeli, M., Tomson, G., Woodhouse, W., Ombaka, E., Peralta, A. Q., Qamar, F. N., Mir, F., Kariuki, S., Bhutta, Z. A., Coates, A., Bergstrom, R., Wright, G. D., Brown, E. D. and Cars. O. (2013). Antibiotic resistance—the need for global solutions. The Lancet Infectious Diseases, 13(12), 1057-1098.

O'Donnell, K., Sutton, D.A., Rinaldi, M.G., Gueidan, C., Crous, P.W. and Geiser, D.M. (2009). Novel multilocus sequence typing scheme reveals high genetic diversity of human pathogenic members of the Fusarium incarnatum-F. equiseti and F. chlamydosporum species complexes within the United States. Journal of Clinical Microbiology. 47(12), 3851-3861.

O’Gorman, C.M. (2011). Airborne Aspergillus fumigatus conidia: a risk factor for aspergillosis. Fungal Biology Reviews, 25(3), 151-157.

Palmieri, S., Pellegrini, M., Ricci, A., Compagnone, D. and Lo Sterzo, C. (2020). Chemical composition and antioxidant activity of thyme, hemp and coriander extracts: A comparison study of maceration, Soxhlet, UAE and RSLDE techniques. Foods, 9(9):1221.

Pawar, V. C. and Thaker, V. S. (2006). In vitro efficacy of 75 essential oils against Aspergillus niger. Mycoses. 49 (4), 316-323.

Peay, K. G., Kennedy, P. G., and Talbot, J. M. (2016). Dimensions of biodiversity in the Earth mycobiome. Nature Reviews Microbiology. 14(7): 434-447.

Qadir, M. I. and Ahmad, Z. (2017). Advances in hepatoprotective medicinal plants research. ||| Bangladesh Journal of Pharmacology|||, 12(3):229-242.

Qari, S. H., Shi, Y. P., Pieniazek, N. J., Collins, W. E. and Lal, A. A. (1996). Phylogenetic relationship among the malaria parasites based on small subunit rRNA gene sequences: monophyletic nature of the human malaria parasite, Plasmodium falciparum1. Molecular Phylogenetics and Evolution. 6(1), 157-165.

Ramasamy, R. (2014). Zoonotic malaria–global overview and research and policy needs. Frontiers in Public Health, 2:123.

Remmal, A., Bouchikhi, T., Rhayour, K., Ettayebi, M. and Tantaoui-Elaraki, A. (1993). Improved method for the determination of antimicrobial activity of essential oils in agar medium. Journal of Essential Oil Research. 5(2):179-184.

Sagar, N. A., Pareek, S., Sharma, S., Yahia, E. M. and Lobo, M. G. (2018). Fruit and vegetable waste: bioactive compounds, their extraction, and possible utilization. Comprehensive Reviews in Food Science and Food Safety, 17(3), 512-531.

Salah, H., Al-Hatmi, A.M., Theelen, B., Abukamar, M., Hashim, S., van Diepeningen, A.D., Lass-Flörl, C., Boekhout, T., Almaslamani, M. and Taj-Aldeen, S.J. (2015). Phylogenetic diversity of human pathogenic Fusarium and emergence of uncommon virulent species. Journal of Infection, 71(6), 658-666.

Sankeshwari, R. M., Ankola, A. V., Bhat, K. and Hullatti, K. (2018). Soxhlet versus cold maceration: which method gives better antimicrobial activity to licorice extract against: Streptococcus Mutans?. Journal of the Scientific Society. 45(2), 67-71.

Schroers, H. J., O’Donnell, K., Lamprecht, S. C., Kammeyer, P. L., Johnson, S., Sutton, D. A., Rinaldi, M. G., Geiser, D. M. and Summerbell, R. C. (2009). Taxonomy and phylogeny of the Fusarium dimerum species group. Mycologia. 101(1), 44-70.

Schwalbe, R., Steele-Moore, L., and Goodwin, A.C. (2007). Antimicrobial susceptibility testing protocols. CRC Press, Boca Raton, Florida.

Sharp, P. M., Plenderleith, L. J. and Hahn, B. H. (2020). Ape origins of human malaria. Annual Review of Microbiology, 74:39.

Spagnuolo, M., Yaguchi, A. and Blenner, M. (2019). Oleaginous yeast for biofuel and oleochemical production. Current Opinion in Biotechnology, 57, 73-81.

Sridhar, A., Ponnuchamy, M., Kumar, P. S., Kapoor, A., Vo, D. V. N., and Prabhakar, S. (2021). Techniques and modeling of polyphenol extraction from food: a review. Environmental Chemistry Letters, 19, 3409-3443.

Szabo, K., Teleky, B. E., Ranga, F., Roman, I., Khaoula, H., Boudaya, E., Ben Ltaief, A., Aouani, W., Thiamrat, M. and Vodnar, D.C. (2022). Carotenoid recovery from tomato processing by-products through green chemistry. Molecules, 27(12):3771.

Venkatesan, D. and Karrunakaran, C. M. (2010). Antimicrobial activity of selected Indian medicinal plants. Journal of Phytology. 2(2):44-48.

Yu, R., Liu, J., Wang, Y., Wang, H. and Zhang, H. (2021). Aspergillus niger as a secondary metabolite factory. Frontiers in Chemistry. 9.

Zhang, Q., Liu, F., Zeng, M., Mao, Y. and Song, Z. (2021). Drug repurposing strategies in the development of potential antifungal agents. Applied Microbiology and Biotechnology. 105(13), 5259-5279.



DOI: https://doi.org/10.22146/ifnp.79710

Article Metrics

Abstract views : 1026 | views : 589

Refbacks

  • There are currently no refbacks.


Creative Commons License
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.

Indonesian Food and Nutrition Progress (print ISSN 0854-6177, online ISSN 2597-9388) is published by the Indonesian Association of Food Technologist in collaboration with Department of Food and Agricultural Product Technology, Faculty of Agricultural Technology, Universitas Gadjah Mada.

Journal of Indonesian Food and Nutrition Progress have been indexed by: 

   

 

This works is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.