Sains Malaysiana 50(9)(2021): 2563-2577

http://doi.org/10.17576/jsm-2021-5009-06

Biological Activities and Chemical Profiles of Selected Soil Fungi Isolated from Sirindhorn Peat Swamp Forest of Narathiwat, Thailand

(Aktiviti Biologi dan Profil Kimia Kulat Tanah Terpilih yang Dipencilkan dari Hutan Paya Gambut Sirindhorn di Narathiwat, Thailand)

SUKANYA DEJ-ADISAI*, NARISORN KAEWCHUTIMA, CHATCHAI WATTANAPIROMSAKUL & SATHIANPONG PHOOPHA

Department of Pharmacognosy and Pharmaceutical Botany, Faculty of Pharmaceutical Sciences, Prince of Songkla University, Songkhla 90112, Thailand

Diserahkan: 3 Februari 2020/Diterima: 6 Januari 2021

ABSTRACT

A total of 54 soil fungi were collected from Sirindhorn peat swamp forest in Narathiwat Province which is the last peat swamp forests in Thailand. They were extracted using four different solvents and 104 crude extracts were obtained. The bioactivity screening of these samples was done employing alpha-glucosidase inhibition, anti-inflammation using nitric oxide inhibition and cytotoxicity using cancer cell line (MCF-7). The results showed that SPSF224 crude extract had the best biological activities in the screening tests and was then selected for further study. The SPSF224 was identified as Penicillium maximae. The crude extracts of P. maximae were determined for chemical profile, IC₅₀ value of alpha-glucosidase inhibition, antioxidant and antimicrobial activities against Staphylococcus aureus, Trichophyton mentagrophytes, and T. rubrum. This was the first report of chemical investigation and biological activity evaluation of P. maximae.

Keywords: Alpha-glucosidase inhibition; antidiabetic; anti-microbial; antioxidant; Penicillium maximae

ABSTRAK

Sebanyak 54 kulat tanah telah dikumpulkan daripada hutan paya gambut Sirindhorn di Wilayah Narathiwat yang merupakan hutan paya gambut terakhir di Thailand. Kesemuanya diekstrak menggunakan empat pelarut yang berbeza dan 104 ekstrak kasar diperoleh. Penyaringan bioaktiviti sampel ini dilakukan dengan menggunakan aktiviti perencatan alfa-glukosidase, anti-radang menggunakan perencatan nitrik oksida dan sitotoksisita menggunakan titisan sel kanser (MCF-7). Hasil kajian menunjukkan bahawa ekstrak kasar SPSF224 mempunyai aktiviti biologi terbaik dalam ujian saringan dan kemudian dipilih untuk kajian lebih lanjut. SPSF224 dikenal pasti sebagai Penicillium maximae. Ekstrak kasarP. maximae ditentukan untuk profil kimia, nilai IC₅₀ perencatan alfa-glukosidase, aktiviti antioksida dan antimikrob terhadapStaphylococcus aureus, Trichophyton mentagrophytes dan T. rubrum. Ini adalah laporan pertama penyelidikan kimia dan penilaian aktiviti biologiP. maximae.

Kata kunci:      Antidiabetik; antimikrob; antioksidan; Penicillium maximae; perencatan alfa-glukosidase

RUJUKAN

Artanti, N., Tachibana, S., Kardono, L.B. & Sukiman, H. 2012. Isolation of alpha-glucosidase inhibitors produced by an endophytic fungus, Colletotrichum sp. TSC13 from Taxus sumatrana. Pakistan Journal of Biological Sciences 15(14): 673-679.

Bischoff, H. 1994. Pharmacology of a‐glucosidase inhibition. European Journal of Clinical Investigation 24(3): 3-10.

Bhardwaj, A., Sharma, D., Jadon, N. & Agrawal, P.K. 2015. Antimicrobial and phytochemical screening of endophytic fungi isolated from spikes of Pinus roxburghii. Archives of Clinical Microbiology 6(3): 1-9.

Boonyuen, N., Sri-Indrasutdhi, V., Suetrong, S., Sivichai, S. & Jones, E.G. 2012. Annulatascus aquatorba sp. nov., a lignicolous freshwater ascomycete from Sirindhorn peat swamp forest, Narathiwat, Thailand. Mycologia 104(3): 746-757.

Brunati, M., Rojas, J.L., Sponga, F., Ciciliato, I., Losi, D., Göttlich, E. & Marinelli, F. 2009. Diversity and pharmaceutical screening of fungi from benthic mats of Antarctic lakes. Marine Genomics 2(1): 43-50.

Bureau of Non Communicable Disease (NCD). 2019. The Number of Thais with Diagnosed Diabetes.www.thaincd.com/2016/mission/documents.php. Accessed on December 24, 2019.

Casqueiro, J. & Alves, C. 2012. Infections in patients with diabetes mellitus: A review of pathogenesis. Indian Journal of Endocrinology and Metabolism 16(Suppl1): S27.

Cazar, M., Schmeda-Hirschmann, G. & Astudillo, L. 2005. Anti-microbial butyrolactone I derivatives from the Ecuadorian soil fungus Aspergillus terreus Thorn. var terreus. World Journal of Microbiology and Biotechnology 21(6-7): 1067-1075.

Chandra, P. & Arora, D.S. 2012. Optimization of antioxidant potential of Penicillium granulatum Bainier by statistical approaches. International Scholarly Research Notices Microbiology2012(1): 452024.

Chang, C.C., Yang, M.H., Wen, H.M. & Chern, J.C. 2002. Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food and Drug Analysis 10(3): 178-182.

Dej-adisai, S. & Pitakbut, T. 2015. Determination of a-glucosidase inhibitory activity from selected Fabaceae plants. Pakistan Journal of Pharmaceutical Sciences 28(5): 1679-1683.

Dej-adisai, S., Phoopha, S. & Puripattanavong, J. 2018. Phytochemical investigation and bioactivities of Alternanthera ramosissima (Mart.) Chodat and Hassl. Pharmacognosy Magazine 14(57): 346-351.

Deshmukh, S.K., Mishra, P.D., Kulkarni-Almeida, A., Verekar, S., Sahoo, M.R., Periyasamy, G., Goswami, H., Khanna, A., Balakrishnan, A. & Vishwakarma, R. 2009. Anti-inflammatory and anticancer activity of ergoflavin isolated from an endophytic fungus. Chemistry & Biodiversity 6(5): 784-789.

Devi, N.N., Prabakaran, J.J. & Wahab, F. 2012. Phytochemical analysis and enzyme analysis of endophytic fungi from Centella asiatica. Asian Pacific Journal of Tropical Biomedicine 2(3): 1280-1284.

Dighton, J. & White, J.F. 2017. The Fungal Community: Its Organization and Role in the Ecosystem. Boca Raton: CRC Press.

Do Rosário Marinho, A.M., Rodrigues-Filho, E., Maria da Luz, R.M. & Santos, L.S. 2005. Biologically active polyketides produced by Penicillium janthinellum isolated as an endophytic fungus from fruits of Melia azedarach. Journal of the Brazilian Chemical Society 16(2): 280-283.

Farnsworth, N.R. 1966. Biological and phytochemical screening of plants. Journal of Pharmaceutical Sciences 55(3): 225-276.

Fuchs, P., Perez-Pinzon, M.A. & Dave, K.R. 2013. Cerebral ischemia in diabetics and oxidative stress. In Diabetes: Oxidative Stress and Dietary Antioxidants.Elsevier Inc. pp. 15-23.

Gao, H., Huang, Y.N., Gao, B., Xu, P.Y., Inagaki, C. & Kawabata, J. 2008. Α-glucosidase inhibitory effect by the flower buds of Tussilago farfara L. Food Chemistry 106(3): 1195-1201.

George, T.K., Devadasan, D. & Jisha, M.S. 2019. Chemotaxonomic profiling of Penicillium setosum using high-resolution mass spectrometry (LC-Q-ToF-MS). Heliyon 5(9): e02484.

Hakamata, W., Kurihara, M., Okuda, H., Nishio, T. & Oku, T. 2009. Design and screening strategies for a-glucosidase inhibitors based on enzymological information. Current Topics in Medicinal Chemistry 9(1): 3-12.

Harborne, J.B. 1984. Methods of plant analysis. Phytochemical Methods. Dordrecht: Springer. Dordrecht pp. 1-36.

Horii, S., Fukase, H., Matsuo, T., Kameda, Y., Asano, N. & Matsui, K. 1986. Synthesis and. alpha-D-glucosidase inhibitory activity of N-substituted valiolamine derivatives as potential oral antidiabetic agents. Journal of Medicinal Chemistry 29(6): 1038-1046.

Huang, D., Ou, B. & Prior, R.L. 2005. The chemistry behind antioxidant capacity assays. Journal of Agricultural and Food Chemistry 53(6): 1841-1856.

Jakovljević, V.D., Milićević, J.M., Stojanović, J.D., Solujić, S.R. & Vrvić, M.M. 2014. Antioxidant activity of ethanolic extract of Penicillium chrysogenum and Penicillium fumiculosum. Hemijska Industrija 68(1): 43-49.

Kalinina, S.A., Kalinin, D.V., Hövelmann, Y., Daniliuc, C.G., Mück-Lichtenfeld, C., Cramer, B. & Humpf, H.U. 2018. Auranthine, a benzodiazepinone from Penicillium aurantiogriseum: Refined structure, absolute configuration, and cytotoxicity. Journal of Natural Products81(10): 2177-2186.

Kalra, S. 2014. Alpha glucosidase inhibitors. The Journal of the Pakistan Medical Association 64(4): 474-476.

Lai, D., Brötz-Oesterhelt, H., Müller, W.E., Wray, V. & Proksch, P. 2013. Bioactive polyketides and alkaloids from Penicillium citrinum, a fungal endophyte isolated from Ocimum tenuiflorum. Fitoterapia 91: 100-106.

Lorian, V. 2005. Antibiotics in Laboratory Medicine. 5th ed. Philadelphia: Lippincott Williams & Wilkins.

MacMillan, J. 1954. Griseofulvin. Part IX. Isolation of the bromo-analogue from Penicillium griseofulvum and Penicillium nigricans. Journal of the Chemical Society (Resumed) 1954: 2585-2587.

Marinho, A.M., Marinho, P.S., Santos, L.S., Rodrigues Filho, E. & Ferreira, I.C. 2013. Active polyketides isolated from Penicillium herquei. Anais da Academia Brasileira de Ciências 85(3): 909-912.

Montefusco-Pereira, C.V., de Carvalho, M.J., de Araújo Boleti, A.P., Teixeira, L.S., Matos, H.R. & Lima, E.S. 2013. Antioxidant, anti-inflammatory, and hypoglycemic effects of the leaf extract from Passiflora nitida Kunth. Applied Biochemistry and Biotechnology 170(6): 1367-1378.

Office of the Royal Development Projects Board (ORDPB) 2019. Pa Phru to Daeng. www.rdpb.go.th/th. Accessed on September 15, 2019.

Rukachaisirikul, V., Rungsaiwattana, N., Klaiklay, S., Pakawatchai, C., Saithong, S., Phongpaichit, S., Borwornwiriyapan, K. & Sakayaroj, J. 2013. Indole-benzodiazepine-2, 5-dione derivatives from a soil fungus Aspergillus sp. PSU-RSPG185. Tetrahedron 69(52): 11116-11121.

Sadananda, T., Govindappa, M., Vinay Dutt, G., Bhat, B., Baishya, P. & Chandrappa, C. 2014. Isolation and characterization of antiviral and ribosome inactivating protein from the endophytic fungi Alternaria sp. from Viscum album using MADLI-TOF-MS and their antibacterial activity. Drug Invention Today 6(2): 105-112.

Schoch, C.L., Seifert, K.A., Huhndorf, S., Robert, V., Spouge, J.L., Levesque, C.A., Chen, W. & Consortium, F.B. 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proceedings of the National Academy of Sciences of the United States of America 109(16): 6241-6246.

Scott, J.A. & King, G.L. 2004. Oxidative stress and antioxidant treatment in diabetes. Annals of the New York Academy of Sciences 1031(1): 204-213.

Shwab, E.K. & Keller, N.P. 2008. Regulation of secondary metabolite production in filamentous ascomycetes. Mycological Research 112(2): 225-230.

Shweta, S., Ritesh, T., Khadabadi, S.S. & Deokate, U.A. 2010. In vitro antioxidant activity and total phenolic, flavonoid contents of the crude extracts of Pterospermum acerifolium Willd leaves (Sterculiaceae). Journal of Chemical and Pharmaceutical Research 2(3): 417-423.

Sikandar, A., Zhang, M., Wang, Y., Zhu, X., Liu, X., Fan, H. & Duan, Y. 2020. Mycochemical screening and analysis, antioxidant activity, and biochemical composition of fermentation strain Snef1216 (Penicillium chrysogenum). Journal of Analytical Methods in Chemistry 2020(2): 1-8.

Singleton, V.L. & Rossi, J.A. 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture 16(3): 144-158.

Tang, H.Y., Zhang, Q., Li, H. & Gao, J.M. 2015. Antimicrobial and allelopathic metabolites produced by Penicillium brasilianum. Natural Product Research 29(4): 345-348.

Thawai, C. 2004. Taxonomy of Micromonospora strains from Thai peat swamp forest soils and secondary metabolites of a selected isolate. PhD. Thesis. Chulalongkorn University (Unpublished).

Tomoda, H., Tabata, N., Masuma, R., Si, S.Y. & Omura, S. 1998. Erabulenols, inhibitors of cholesteryl ester transfer protein produced by Penicillium sp. FO-5637. The Journal of Antibiotics 51(7): 618-623.

Trease, G.E. & Evans, W.C. 1983. Textbook of Pharmacognosy. 12th ed. London: Balliers Tindall. pp. 343-384.

Trisuwan, K., Rukachaisirikul, V., Borwornwiriyapan, K., Phongpaichit, S. & Sakayaroj, J. 2014. Benzopyranone, benzophenone, and xanthone derivatives from the soil fungus Penicillium citrinum PSU-RSPG95. Tetrahedron Letters 55(7): 1336-1338.

Trisuwan, K., Rukachaisirikul, V., Kaewpet, M., Phongpaichit, S., Hutadilok-Towatana, N., Preedanon, S. & Sakayaroj, J. 2011. Sesquiterpene and xanthone derivatives from the sea fan-derived fungus Aspergillus sydowii PSU-F154. Journal of Natural Products 74(7): 1663-1667.

Turbyville, T.J., Wijeratne, E.K., Liu, M.X., Burns, A.M., Seliga, C.J., Luevano, L.A., David, C.L., Faeth, S.H., Whitesell, L. & Gunatilaka, A.L. 2006. Search for Hsp90 inhibitors with potential anticancer activity: Isolation and SAR studies of radicicol and monocillin I from two plant-associated fungi of the Sonoran desert. Journal of Natural Products 69(2): 178-184.

Visagie, C.M., Houbraken, J., Frisvad, J.C., Hong, S.B., Klaassen, C.H.W., Perrone, G., Seifert, K.A., Varga, J., Yaguchi, T. & Samson, R.A. 2014. Identification and nomenclature of the genus Penicillium. Studies in Mycology 78: 343-371.

Visagie, C.M., Houbraken, J., Rodriques, C., Pereira, C.S., Dijksterhuis, J., Seifert, K.A., Jacobs, K. & Samson, R.A. 2013. Five new Penicillium species in section Sclerotiora: A tribute to the Dutch Royal family. Persoonia 31: 42-62.

Wang, P.L., Li, D.Y., Xie, L.R., Wu, X., Hua, H.M. & Li, Z.L. 2014. Two new compounds from a marine-derived fungus Penicillium oxalicum. Natural Product Research 28(5): 290-293.

Wang, X., You, J., King, J.B., Powell, D.R. & Cichewicz, R.H. 2012. Waikialoid a suppresses hyphal morphogenesis and inhibits biofilm development in pathogenic Candida albicans. Journal of Natural Products 75(4): 707-715.

Waring, P., Eichner, R.D., Tiwari-Palni, U. & Mullbacher, A. 1987. Gliotoxin-E: A new biologically-active epipolythiodioxopiperazine isolated from Penicillium terlikowskii. Australian Journal of Chemistry 40(5): 991-997.

World Health Organization (WHO). 2019. Guidelines on Second-and Third-Line Medicines and Type of Insulin for the Control of Blood Glucose Levels in Non-Pregnant Adults with Diabetes Mellitus. http://apps.who.int/iris/bitstream/handle/10665/272433. Accessed July 7, 2019.

Zhao, J., Li, C., Wang, W., Zhao, C., Luo, M., Mu, F., Fu, Y., Zu, Y. & Yao, M. 2013. Hypocrea lixii, novel endophytic fungi producing anticancer agent cajanol, isolated from pigeon pea (Cajanus cajan [L.] M illsp.). Journal of Applied Microbiology 115(1): 102-113.

*Pengarang untuk surat-menyurat; email: sukanya.d@psu.ac.th