Evaluation of Fomitopsis betulina strains for growth on different media and exopolysaccharide production
DOI:
https://doi.org/10.2298/ABS240523018KKeywords:
Birch polypore, biomass, media, mycelium, exopolysaccharideAbstract
Paper description:
- Fomitopsis betulina fungus has valuable medicinal potential. We screened 22 different betulina strains for mycelial growth on different media and exopolysaccharide production.
- Growth in agar media was measured by radial growth rate, and growth in liquid media by biomass dry weight/L. The crude exopolysaccharide content was examined by the phenol-sulfuric acid method.
- The importance of growth media and fungal strains in the production of biomass and exopolysaccharides is shown.
- The study helps establish optimal protocols for cultivating betulina in laboratory and industrial settings.
Abstract: Fomitopsis betulina is a widespread macromycete with valuable medicinal potential. This study screened 22 different F. betulina strains for mycelial growth on various media and exopolysaccharide production. Strain-specific features of F. betulina growth and exopolysaccharide production on different media were observed. Variations in the growth rate of the studied strains ranged from 3.50±0.33 to 8.75±0.50 mm/day, biomass synthesis from 2.28±0.26 to 13.72±0.05 g/L, and exopolysaccharide production from 0.02±0.00 to 2.20±0.31 g/L. Maltose as a carbon source in malt extract agar (MEA) and malt extract broth (MEB) was the most suitable for the growth, while dextrose and starch as carbon sources in potato dextrose broth (PDB) were more suitable for exopolysaccharide production. The F. betulina 311 strain has significant biotechnological potential, demonstrated by its robust growth on different agar media, efficient biomass synthesis, and high production of extracellular biopolymers. Our results highlight the significance of different growth media and fungal strains in optimizing biomass and exopolysaccharide production.
Downloads
References
Lemieszek ML, Langner E, Kaczor J, Kandefer-Szerszen M, Sanecka B, Mazurkiewicz W, Rzeski W. Anticancer effect of fraction isolated from medicinal Birch polypore mushroom, Piptoporus betulinus (Bull.: Fr.) P. Karst (Aphyllophoromycetideae): in vitro studies. Int J Med Mushrooms. 2009;11(4): 351-64. https://doi.org/10.1615/IntJMedMushr.v11.i4.20
Grienke U, Zöll M, Peintner U, Rollinger JM. European medicinal polypores – a modern view on traditional uses. J Ethnopharmacol. 2014;154(3):564-83. https://doi.org/10.1016/j.jep.2014.04.030
Guthmann J. Medicinal mushrooms: a portrait of the world's most important species. 2nd ed. Wiebelsheim: Quelle & Meyer Verlag; 2016. German.
Pleszczyńska M, Lemieszek MK, Siwulski M, Wiater A, Rzeski W, Szczodrak J. Fomitopsis betulina (formerly Piptoporus betulinus): the Iceman's polypore fungus with modern biotechnological potential. World J Microbiol Biotechnol. 2017;33(83):1-12. https://doi.org/10.1007/s11274-017-2247-0
Gründemann C, Reinhardt JK, Lindequist U. European medicinal mushrooms: do they have potential for modern medicine? An update. Phytomedicine. 2019;66:153131. https://doi.org/10.1016/j.phymed.2019.153131
Gafforov Y, Deshmuk SK, Verekar SA, Tomšovský M, Yarasheva M, Chen JJ, Langer E, Rapior S. Fomitopsis betulina (Bull.) B.K. Cui, M.L. Han & Y.C. Dai; Fomitopsis pinicola (Sw.) P. Karst. – Fomitopsidaceae. In: Khojimatov OK, Gafforov Y, Bussmann RW, editors. Ethnobiology of Uzbekistan. Ethnobiology. Cham: Springer; 2023. p. 1085-101. https://doi.org/10.1007/978-3-031-23031-8_108
Rutalek R. Ethnomycology – An Overview. Osterr Z Pilzkd. 2002;11:79-94. German.
Papp N, Rudolf K, Bencsik T, Czégényi D. Ethnomycological use of Fomes fomentarius (L.) Fr. and Piptoporus betulinus (Bull.) P. Karst. in Transylvania, Romania. Genet Resour Crop Evol. 2017;64:101-11. https://doi.org/10.1007/s10722-015-0335-2
Zwolińska K. Evaluation of anticancer activity of extracts from birch polypore Piptoporus betulinus (Bull. ex Fr.) P. Karst. [dissertation]. Lublin: Maria Curie-Skłodowska University; 2004.
Cyranka M, Graz M, Kaczor J, Kandefer-Szerszen M, Walczak K, Kapka-Skrzypczak L, Rzeski W. Investigation of antiproliferative effect of ether and ethanol extracts of birch polypore medicinal mushroom, Piptoporus betulinus (Bull.:Fr.) P. Karst. (higher Basidiomycetes) in vitro grown mycelium. Int J Med Mushrooms. 2011;13(6):525-33. https://doi.org/10.1615/intjmedmushr.v13.i6.40
Sułkowska-Ziaja K, Szewczyk A, Galanty A, Gdula-Argasińska J, Muszyńska B. Chemical composition and biological activity of extracts from fruiting bodies and mycelial cultures of Fomitopsis betulina. Mol Biol Rep. 2018;45(6):2535–44. https://doi.org/10.1007/s11033-018-4420-4
Khalilov Q, Li L, Liu Y, Tohtahon Z, Chen X, Aisa HA, Yuan T. Piptolinic acids F-J, five new lanostane-type triterpenoids from Piptoporus betulinus. Nat Prod Res. 2018;33(21):3044-51. https://doi.org/10.1080/14786419.2018.1516218
Weber LA, Puff C, Kalbitz J, Kietzmann M, Feige K, Bosse K, Rohn K, Cavalleri JV. Concentration profiles and safety of topically applied betulinic acid and NVX-207 in eight healthy horses – A randomized, blinded, placebo-controlled, crossover pilot study. J Vet Pharmacol Ther. 2020;44(1):47-57. https://doi.org/10.1111/jvp.12903
Schlegel B, Luhmann U, Haertl A, Graefe U. Piptamine, a new antibiotic produced by Piptoporus betulinus Lu 9-1. J Antibiot (Tokyo). 2000;53(9):973–4. https://doi.org/10.7164/antibiotics.53.973
Keller AC, Maillard MP, Hostettmann K. Antimicrobial steroids from the fungus Fomitopsis pinicola. Phytochemistry. 1996;41(4):1041-6. https://doi.org/10.1016/0031-9422(95)00762-8
Alresly Z, Lindequist U, Lalk M, Porzel A, Arnold N, Wessjohann LA. Bioactive triterpenes from the fungus Piptoporus betulinus. Rec Nat Prod. 2016;10(1):103-8.
Alresly Z. Chemical and pharmacological investigations of Fomitopsis betulina (formerly: Piptoporus betulinus) and Calvatia gigantea [dissertation]. Greifswald: Universität of Greifswald; 2019. https://doi.org/10.13140/RG.2.2.27835.54561
Krupodorova TA, Barshteyn VYu, Zabeida EF, Pokas EV. Antibacterial activity of macromycetes mycelia and culture liquid. Microbiol Biotechnol Lett. 2016;44(3):246-53. https://doi.org/10.4014/mbl.1603.03003
Krupodorova T, Barshteyn V, Kizitska T, Kvasko H, Andriiash H, Tigunova O. Effect of ultraviolet C irradiation on growth and antibacterial activity of Fomitopsis betulina (Bull.) B.K. Cui, M.L. Han and Y.C. Dai. GSC Biol Pharm Sci. 2018;04(03):001–6. https://doi.org/10.30574/gscbps.2018.4.3.0073
Krupodorova TA, Barshteyn VYu, Kizitska TO, Pokas EV. Effect of cultivation conditions on mycelial growth and antibacterial activity of Lentinula edodes and Fomitopsis betulina. Czech Mycol. 2019;71(2):167-86. https://doi.org/10.33585/cmy.71204
Verekar SA, Gupta MK, Deshmukh SK. Fomitopsis betulina a rich source of diverse bioactive metabolites. In: Sridhar KR, Deshmukh SK editors. Advances in macrofungi. Pharmaceuticals and cosmeceuticals. Boca Raton: CRC Press; 2021. p. 22-66. https://doi.org/10.1201/9781003191278
Vunduk J, Klaus A, Kozarski M. Petrovic P, Zizak Z, Niksic M, Van Griensven LJ. Did the Iceman know better? Screening of the medicinal properties of the Birch polypore medicinal mushroom, Piptoporus betulinus (higher Basidiomycetes). Int J Med Mushrooms. 2015;17(12):1113-25. https://doi.org/10.1615/intjmedmushrooms.v17.i12.10
de Jesus LI, Smiderle FR, Ruthes AC, Vilaplana F, Dal'Lin FT, Maria-Ferreira D, Werner MF, Van Griensven L, Iacomini M. Chemical characterization and wound healing property of a β-D-glucan from edible mushroom Piptoporus betulinus. Int J Biol Macromol. 2018;117:1361-6. https://doi.org/10.1016/j.ijbiomac.2017.12.107
Grunewald F, Steinborn C, Huber R, Wille R, Meier S, Alresly Z, Lindequist U, Gründemann C. Effects of Birch polypore mushroom, Piptoporus betulinus (Agaricomycetes), the "Iceman's Fungus", on human immune cells. Int J Med Mushrooms. 2018;20(12):1135-47. https://doi.org/10.1615/IntJMedMushrooms.2018029154
Sofrenić I, Anđelković B, Todorović N, Stanojković T, Vujisić L, Novaković M, Milosavljević S, Tešević V. Cytotoxic triterpenoids and triterpene sugar esters from the medicinal mushroom Fomitopsis betulina. Phytochemistry. 2021;181:112580. https://doi.org/10.1016/j.phytochem.2020.112580
Wiater A, Paduch R, Plesczyńska M, Pŕochniak K, Choma A, Kandefer-Szerszeń M, Szczodrak J. α-(1 → 3)-D-Glucans from fruiting bodies of selected macromycetes fungi and the biological activity of their carboxymethylated products. Biotechnol Lett. 2001;33:787-95. https://doi.org/10.1007/s10529-010-0502-7
Mykhaylova OB. Morphological and cultural properties of a medicinal mushroom, Piptoporus betulinus (Basidiomycetes), on nutrient agar media. Ukr Bot J. 2014;71(5):603-9. Ukrainian. https://doi.org/10.15407/ukrbotj71.05.603
Badalyan SM, Gharibyan NG. Characteristics of mycelial structures of different fungal collections – Yerevan: YSU Press, 2017, p. 176.
Mykchaylova O, Lomberg M, Krasinko V. Biotechnological basis of intensive cultivation of medicinal mushroom Fomitopsis betulina (Fomitopsidaceae, Polyporales). Sci Works NUFT. 2021;27(1):32-41. Ukrainian.
Mensah D, Obodai M. Morphological characteristics of mycelial growth of two strains of the indigenous medicinal mushroom, Lentinus squarrosulus Mont. (Singer), on solid media. Afr J Agric Res. 2014;9(23):1753-60. https://doi.org/10.5897/AJAR2013.8340
Zerva A, Tsafantakis N, Topakas E. Evaluation of Basidiomycetes wild strains grown in agro-industrial residues for their anti-tyrosinase and antioxidant potential and for the production of biocatalysts. Fermentation (Basel). 2021;7(1):19. https://doi.org/10.3390/fermentation7010019
Krupodorova T, Barshteyn V, Tsygankova V, Sevindik M, Blume Y. Strain-specific features of Pleurotus ostreatus growth in vitro and some of its biological activities. BMC Biotechnol. 2024;24:9. https://doi.org/10.1186/s12896-024-00834-9
Bisko N, Lomberg M, Mykhaylova O, Mytropolska N. IBK Mushroom Culture Collection [Internet]. Version 1.8. Copenhagen (Denmark): GBIF Norway; 2024 Feb 24 [cited 2024 Apr 29]. Available from: https://doi.org/10.15468/dzdsqu
Weis AL, Solomko EF, Buchalo AS, Wasser SP, Mitropolskaya NYu, Grigansky APh, Gorovits EL. Cultural study and illudin S production of medicinal mushroom Omphalotus olearius (DC.: Fr.) Fay. (Agaricales s.l.) from Israel. Int J Med Mushrooms. 1999;1(1):93-103. https://doi.org/10.1615/IntJMedMushrooms.v1.i1.80
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem. 1956;28(3):350-6. https://doi.org/10.1021/ac60111a017
Evans JD. Straightforward statistics for the behavioral sciences. Pacific Grove: Brooks/Cole Pub. Co.; 1996.
Badalyan SM, Gharibyan NG, Iotti M, Zambonelli A. Morphological and ecological screening of different collections of medicinal white-rot bracket fungus Ganoderma adspersum (Schulzer) Donk (Agaricomycetes, Polyporales). Ital J Mycol. 2019;48:1-15. https://doi.org/10.6092/issn.2531-7342/9092
Krupodorova T, Barshteyn V, Al-Maali G, Sevindik M. Requirements for vegetative growth of Hohenbuehelia myxotricha and its antimycotic activity. Pol J Natur Sc. 2022;7(1):75-92.
Badalyan S, Gharibyan N, Gianchino C, Iotti M, Zambonelli A. Morphological observation and biomass formation in different edible medicinal Morchella collections (Pezizomycetes, Ascomycota). Ital J Mycol. 2023;52(1):50-61. https://doi.org/10.6092/issn.2531-7342/16112
Guadarrama-Mendoza PC, del Toro GV, Ramírez-Carrillo R, Robles-Martínez F, Yáñez-Fernández J, Garín-Aguilar ME, Hernández CG, Bravo-Villa G. Morphology and mycelial growth rate of Pleurotus spp. strains from the Mexican mixtec region. Braz J Microbiol. 2014; 45(3):861-72. https://doi.org/10.1590/s1517-83822014000300016
Dzhagan V, Krupodorova T, Atamanchuk A, Lytvynenko Y, Dzhagan V. Growth and morphological characteristics of some pyrophilous discomycetes in culture. Biosyst Divers. 2023;31(3):282-9. https://doi.org/10.15421/012332
Lomberh ML. Medicinal mushrooms in surface and submerged culture [PhD thesis]. Kyiv: M.G. Kholodny Institute of Botany, National Academy of Science; 2005. (In Ukrainian).
Krupodorova T, Barshteyn V, Sekan A. Review of the basic cultivation conditions influence on the growth of basidiomycetes. Curr Res Environ Appl Mycol J Fungal Biol. 2021;1:494-531. https://doi.org/10.5943/cream/11/1/34
Jaros D, Köbsch J, Rohm H. Exopolysaccharides from Basidiomycota: Formation, isolation and techno-functional properties. Eng Life Sci. 2018;18(10):743-52. https://doi.org/10.1002/elsc.201800117
Osemwegie OO, Adetunji CO, Ayeni EA, Adejobi OI, Arise RO, Nwonuma CO, Oghenekaro AO. Exopolysaccharides from bacteria and fungi: current status and perspectives in Africa. Heliyon. 2020;6(6):e04205. https://doi.org/10.1016/j.heliyon.2020.e04205
Osińska-Jaroszuk M, Jarosz-Wilkołazka A, Jaroszuk-Ściseł J, Szałapata K, Nowak A, Jaszek M, Ozimek E, Majewska M. Extracellular polysaccharides from Ascomycota and Basidiomycota: production conditions, biochemical characteristics, and biological properties. World J Microbiol Biotechnol. 2015;31:1823-44. https://doi.org/10.1007/s11274-015-1937-8
Hamidi M, Okoro OV, Milan PB, Khalili MR, Samadian H, Nie L, Shavandi A. Fungal exopolysaccharides: Properties, sources, modifications, and biomedical applications. Carbohydr Polym. 2022;284:119152. https://doi.org/10.1016/j.carbpol.2022.119152
Stoica RM, Moscovici M, Lakatos ES, Cioca LI. Exopolysaccharides of fungal origin: Properties and pharmaceutical applications. Processes. 2023;11(2):335. https://doi.org/10.3390/pr11020335
Lee BC, Bae JT, Pyo HB, Choe TB, Kim SW, Hwang HJ, Yun JW. Submerged culture conditions for the production of mycelial biomass and exopolysaccharides by the edible Basidiomycete Grifola frondose. Enzym Microb Technol. 2004;35(5):369-76. https://doi.org/10.1016/j.enzmictec.2003.12.015
Osińska-Jaroszuk M, Jarosz-Wilkołazka A, Jaroszuk-Ściseł J, Szałapata K, Nowak A, Jaszek M, Ozimek E, Majewska M. Extracellular polysaccharides from Ascomycota and Basidiomycota: production conditions, biochemical characteristics, and biological properties. World J Microbiol Biotechnol. 2015;31(12):1823-44. https://doi.org/10.1007/s11274-015-1937-8
Tavares AP, Agapito MS, Coelho MA, Lopes da Silva JA, Barros-Timmons A, Coutinho JA, Xavier AM. Selection and optimization of culture medium for exopolysaccharide production by Coriolus (Trametes) versicolor. World J Microbiol Biotechnol. 2005;21:1499-507. https://doi.org/10.1007/s11274-005-7370-7
Lin ES, Sung SC. Cultivating conditions influence exopolysaccharide production by the edible Basidiomycete Antrodia cinnamomea in submerged culture. Int J Food Microbiol. 2006;108(2):182-7. https://doi.org/10.1016/j.ijfoodmicro.2005.11.010
Maziero R, Cavazzoni V, Bononi V L R Screening of basidiomycetes for the production of exopolysaccharide and biomass in submerged culture. Revista de Microbiologia. 1999;30:77-84.
Sasidhara R, Bakki V, Thirunalas T Screening of some basidiomycetes for useful polysaccharides. Mushroom Reseearch. 2011;20(2):83-6.
Rajput Y, Shit S, Shukla A, Gupta S, Shukla K Screening for exopolysaccharide production from basidiomycetes of Chhattisgarh. CCCRENT Botany 2011, 2(10):11-14
Umeo SH, Souza GP, Rapachi PM, Garcia DM, Paccola-Meirelles LD, Valle JS, Colauto NB, Linde GA. Screening of basidiomycetes in submerged cultivation based on antioxidant activity. Genet Mol Res. 2015;14(3):9907-14. https://doi.org/10.4238/2015
Montoya S, Sánchez ÓJ, Levin L. Polysaccharide Production by Submerged and Solid-State Cultures from Several Medicinal Higher Basidiomycetes. Int J Med Mushrooms. 2013,15(1): 71–9.
Asadi F, Barshan-Tashnizi M, Hatamian-Zarmi A, Davoodi-Dehaghani F, Ebrahimi-Hosseinzadeh B. Enhancement of exopolysaccharide production from Ganoderma lucidum using a novel submerged volatile co-culture system. Fungal Biol. 2021;125(1):25-31 https://doi.org/10.1016/j.funbio.2020.09.010
Tabibzadeh, F., Alvandi, H., Hatamian-Zarmi, A. et al. Antioxidant activity and cytotoxicity of exopolysaccharide from mushroom Hericium coralloides in submerged fermentation. Biomass Conv. Bioref. 2022. https://doi.org/10.1007/s13399-022-03386-0
Wu C-Y, Liang Z-C, Lu C-P, Wu S-H. Effect of carbon and nitrogen sources on the production and carbohydrate composition of exopolysaccharide by submerged culture of pleurotus citrinopileatus, Journal of Food and Drug Analysis. 2008;16(2):6. https://doi.org/10.38212/2224-6614.2364
Bolla K, Gopinath BV, Shaheen Syed Zeenat, Singara Charya MA. Optimization of carbon and nitrogen sources of submerged culture process for the production of mycelial biomass and exopolysaccharides by Trametes versicolor. Int J Biotechnol Mol.Biol Res. 2010;1(2):15-21.
Mykchaylova O, Dubova H, Lomberg M, Negriyko A, Poyedinok N. Influence of low-intensity light on the biosynthetic activity of the edible medicinal mushroom Hericium erinaceus (Bull.: Fr.) Pers. in vitro. Arch Biol Sci. 2023;75(4):489-501. https://doi.org/10.2298/ABS230821040M
Kim YR. Production of polysaccharide by the edible mushroom, Grifola frondosa. Mycobiology. 2003;31(4):205-8.
Elisashvili V. Submerged cultivation of medicinal mushrooms: bioprocesses and products (Review). Int J Med Mushrooms. 2012;14(3):211-39. https://doi.org/10.1615/intjmedmushr.v14.i3.10
Bisko N, Mustafin K, Al-Maali G, Suleimenova Z, Lomberg M, Narmuratova Z, Mykchaylova O, Mytropolska N, Zhakipbekova A. Effects of cultivation parameters on intracellular polysaccharide production in submerged culture of the edible medicinal mushroom Lentinula edodes. Czech Mycol. 2020;72(1):1-17. https://doi.org/10.33585/cmy.72101
Narmuratova Zh, Bisko N, Mustafin K, Al-Maali G, Kerner A, Bondaruk S, Suleimenova Zh, Kalieva A, Akhmetsadykov N, Zhakipbekova A, Lomberg M. Biological activity of edible medicinal mushrooms of the genus Hericium. Turk J Biochem. 2023;48(3):290-7. https://doi.org/10.1515/tjb-2022-0235
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Tetiana Krupodorova, Tetiana Kizitska, Viсtor Barshteyn, Mustafa Sevindik
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.
