Members of Hymenochaetaceae fungi are among well-known macromycetes with various medicinal properties. The aim of this study was to investigate the biological activities of Phellinus tuberculosus and Fuscoporia ferruginosa collected in Iran. The antimicrobial, antioxidant, and cytotoxic activities of the two species were examined, and their phenolic and polysaccharide contents were quantified. Compounds were characterized by HPLC-DAD chromatography and LC-ESI-MS/MS spectroscopy. According to our results, the antibacterial and antioxidant effects of P. tuberculosus extracts were stronger than F. ferruginosa. Also, the effect of hydroalcoholic extracts was higher than the aqueous extract. Gram-positive bacteria were more sensitive to all extracts, especially Streptococcus mutans with a MIC of 0.7 mg/mL and MBC of 6.25 mg/mL. HPLC-DAD analyses detected gallic acid, caffeic acid, and syringic acid in both fungi. The LC-ESI-MS/MS confirmed the detected compounds in HPLC-DAD and showed the presence of several phenolic compounds such as phellifuropyranone, phelligridin, and hispidin, besides others. This study showed that F. ferruginosa and P. tuberculosus are potent medicinal fungi with antibacterial and antioxidant properties, with no toxic effect on normal HDF cells, and possess various bioactive compounds including styrylpyrone-type phenols with well-known bioactivities.

Department of Biotechnology Iranian Research Organization for Science and Technology Tehran Iran

Department of Chemical Technologies Iranian Research Organization for Science and Technology Tehran Iran

Department of Microbial Biotechnology School of Biology College of Science University of Tehran Tehran Iran

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Abdalla S, Pizzi A, Bahabri F, Ganash A (2015) Analysis of valonia oak (Quercus aegilops) acorn tannin and wood adhesives application. BioResources 10:7165–7177. https://doi.org/10.15376/BIORES.10.4.7165-7177 DOI

Adebayo EA, Martínez-Carrera D, Morales P et al (2018) Comparative study of antioxidant and antibacterial properties of the edible mushrooms Pleurotus levis, P. ostreatus, P. pulmonarius and P. tuber-regium. Int J Food Sci Technol 53:1316–1330. https://doi.org/10.1111/ijfs.13712 DOI

Amin HI, Ibrahim MF, Hussain FH, Sardar AS, Vidari G (2016) Phytochemistry and ethnopharmacology of some medicinal plants used in the Kurdistan region of Iraq. Nat Prod Commun 11:291–296 PubMed

Aryal S, Baniya MK, Danekhu K, Kunwar P, Gurung R, Koirala N (2019) Total phenolic content, flavonoid content and antioxidant potential of wild vegetables from Western Nepal. Plants 8:96. https://doi.org/10.3390/plants8040096 DOI PMC

Ayala-Zavala JF, Silva-Espinoza BA, Cruz-Valenzuela MR et al (2012) Antioxidant and antifungal potential of methanol extracts of Phellinus spp. from Sonora. Mexico Rev Iberoam Micol 29:132–138. https://doi.org/10.1016/j.riam.2011.09.004 PubMed DOI

Chaharmiri Dokhaharani S, Ghobad-Nejhad M, Moghimi H, Farazmand A, Rahmani H (2020) Antibacterial and antioxidant activity of Inocutis levis extracts and evaluation of its polyphenolic compounds. Biol J Microorg 35:1–16. https://doi.org/10.22108/bjm.2020.120139.1240 DOI

Chang H, Ho Y, Sheu M et al (2007) Antioxidant and free radical scavenging activities of Phellinus merrillii extracts. Bot Stud 48:407–417

Chen W, Tan H, Liu Q et al (2019) A review: The bioactivities and pharmacological applications of Phellinus linteus. Molecules 24(10):1888. https://doi.org/10.3390/molecules24101888 DOI PMC

Clinical and Laboratory Standards Institute (2020) Performance Standards for Antifungal Susceptibility Testing of Yeasts. 2nd ed. CLSI supplement M60. Wayne, PA: Clinical and Laboratory Standards Institute

Clinical and Laboratory Standards Institute (2018) Performance standards for antimicrobial susceptibility testing. CLSI supplement M100

Colombo F, Di Lorenzo C, Regazzoni L et al (2019) Phenolic profiles and anti-inflammatory activities of sixteen table grape (Vitis vinifera L.) varieties. Food Funct 10:1797–1807. https://doi.org/10.1039/C8FO02175A PubMed DOI

Cui Y, Kim DS, Park KC (2005) Antioxidant effect of Inonotus obliquus. J Ethnopharmacol 96:79–85. https://doi.org/10.1016/j.jep.2004.08.037 PubMed DOI

Dadgostar P (2019) Antimicrobial resistance: implications and costs. Infect Drug Resist 12:3903. https://doi.org/10.2147/IDR.S234610 PubMed DOI PMC

Dai J, Han R, Xu Y et al (2020) Recent progress of antibacterial natural products: future antibiotics candidates. Bioorg Chem 103922.  https://doi.org/10.1016/j.bioorg.2020.103922

Dai YC (2010) Hymenochaetaceae (Basidiomycota) in China. Fungal Divers 45:131–343. https://doi.org/10.1007/s13225-010-0066-9 DOI

De Silva DD, Rapior S, Sudarman E et al (2013) Bioactive metabolites from macrofungi: ethnopharmacology, biological activities and chemistry. Fungal Divers 62:1–40. https://doi.org/10.1007/s13225-013-0265-2 DOI

Dhage GR, Thopate SR, Ramteke SN, Kulkarni PP (2014) One-pot synthesis and evaluation of novel 3-aryl-6-ethoxycarbonyl-4-hydroxy-2 H-pyran-2-one as a potent cytotoxic agent. RSC Adv 4:56870–56875. https://doi.org/10.1039/C4RA10015H DOI

Ehsanifard Z, Mir-Mohammadrezaei F, Ghobad-Nejhad M, Safarzade AR (2019) The effect of aqueous extract of Inocutis levis on liver histopathology and hypertriglyceridemia in high sucrose-fed Wistar rats. J Med Plants 2:181–187. https://doi.org/10.29252/jmp.2.70.181 DOI

Ehsanifard Z, Mir-Mohammadrezaei F, Safarzadeh A, Ghobad-Nejhad M (2017) Aqueous extract of Inocutis levis improves insulin resistance and glucose tolerance in high sucrose-fed Wistar rats. J Herbmed Pharmacol 6:160–164

Friedman M (2016) Mushroom polysaccharides: chemistry and antiobesity, antidiabetes, anticancer, and antibiotic properties in cells, rodents, and humans. Foods 5:80. https://doi.org/10.3390/foods5040080 DOI PMC

García-Niño WR, Zazueta C (2015) Ellagic acid: pharmacological activities and molecular mechanisms involved in liver protection. Pharmacol Res 97:84–103. https://doi.org/10.1016/j.phrs.2015.04.008 PubMed DOI

Grienke U, Zöll M, Peintner U, Rollinger JM (2014) European medicinal polypores–A modern view on traditional uses. J Ethnopharmacol 154:564–583. https://doi.org/10.1016/j.jep.2014.04.030 PubMed DOI

Han JJ, Bao L, He LW et al (2013) Phaeolschidins A-E, five hispidin derivatives with antioxidant activity from the fruiting body of Phaeolus schweinitzii collected in the Tibetan Plateau. J Nat Prod 76:1448–1453. https://doi.org/10.1021/np400234u PubMed DOI

Hirano Y, Kondo R, Sakai K (2003) 5α-Reductase inhibitory tannin-related compounds isolated from Shorea laeviforia. J Wood Sci 49:339–343. https://doi.org/10.1007/s10086-002-0481-y DOI

Huang GJ, Hsieh WT, Chang HY et al (2011) α-Glucosidase and aldose reductase inhibitory activities from the fruiting body of Phellinus merrillii. J Agric Food Chem 59:5702–5706. https://doi.org/10.1021/jf2003943 PubMed DOI

Huang SC, Wang PW, Kuo PC, Hung HY, Pan TL (2018) Hepatoprotective principles and other chemical constituents from the mycelium of Phellinus linteus. Molecules 23(7):1705. https://doi.org/10.3390/molecules23071705 DOI PMC

Jeon YE (2009) Evaluation of the antioxidant activity of the fruiting body of Phellinus linteus using the on-line HPLC-DPPH method. J Korean Soc Appl Biol Chem 52:472–479. https://doi.org/10.3839/jksabc.2009.081 DOI

Jin QL, Zhang ZF, Lv GY et al (2016) Antioxidant and DNA damage protecting potentials of polysaccharide extracted from Phellinus baumii using a delignification method. Carbohydr Polym 152:575–582. https://doi.org/10.1016/j.carbpol.2016.07.027 PubMed DOI

Johnston GA (2014) Muscimol as an ionotropic GABA receptor agonist. Neurochem Res 39:1942–1947. https://doi.org/10.1007/s11064-014-1245-y PubMed DOI

Kahkeshani N, Farzaei F, Fotouhi M, Alavi SS, Bahramsoltani R et al (2019) Pharmacological effects of gallic acid in health and disease: A mechanistic review. Iran J Basic Med Sci 22: 225–237. https://doi.org/10.22038/ijbms.2019.32806.7897

Kojima K, Ohno T, Inoue M, Mizukami H, Nagatsu A (2008) Phellifuropyranone A: a new furopyranone compound isolated from fruit bodies of wild Phellinus linteus. Chem Pharm Bull 56:173–175. https://doi.org/10.1248/cpb.56.173 DOI

Kuriyama I, Nakajima Y, Nishida H, Konishi T, Takeuchi T et al (2013) Inhibitory effects of low molecular weight polyphenolics from Inonotus obliquus on human DNA topoisomerase activity and cancer cell proliferation. Mol Med Rep 8(2):535–542. https://doi.org/10.3892/mmr.2013.1547 PubMed DOI

Lee IK, Kim YS, Jang YW, Jung JY, Yun BS (2007a) New antioxidant polyphenols from the medicinal mushroom Inonotus obliquus. Bioorg Med Chem Lett 17:6678–6681. https://doi.org/10.1016/j.bmcl.2007.10.072 PubMed DOI

Lee IK, Kim YS, Seok SJ, Yun BS (2007b) Inoscavin E, a free radical scavenger from the fruiting bodies of Inonotus xeranticus. J Antibiot 60:745–747. https://doi.org/10.1038/ja.2007.97 DOI

Lee IK, Han MS, Lee MS, Kim YS, Yun BS (2010) Styrylpyrones from the medicinal fungus Phellinus baumii and their antioxidant properties. Bioorg Med Chem Lett 20:5459–5461. https://doi.org/10.1016/j.bmcl.2010.07.093 PubMed DOI

Lee MS, Hwang BS, Lee IK, Seo GS, Yun BS (2015) Chemical constituents of the culture broth of Phellinus linteus and their antioxidant activity. Mycobiology 43:43–48. https://doi.org/10.5941/MYCO.2015.43.1.43 PubMed DOI PMC

Lee IK, Jung JY, Seok SJ, Kim WG, Yun BS (2006a) Free radical scavengers from the medicinal mushroom Inonotus xeranticus and their proposed biogenesis. Bioorganic Med Chem Lett 16:5621–5624. https://doi.org/10.1016/j.bmcl.2006.08.016 DOI

Lee IK, Seok SJ, Kim WK, Yun BS (2006b) Hispidin derivatives from the mushroom Inonotus xeranticus and their antioxidant activity. J Nat Prod 69:299–301. https://doi.org/10.1021/np050453n PubMed DOI

Lee IK, Yun BS (2011) Styrylpyrone-class compounds from medicinal fungi Phellinus and Inonotus spp., and their medicinal importance. J Antibiot 64:349–359. https://doi.org/10.1038/ja.2011.2 DOI

Matuszewska A, Jaszek M, Stefaniuk D, Ciszewski T, Matuszewski Ł (2018) Anticancer, antioxidant, and antibacterial activities of low molecular weight bioactive subfractions isolated from cultures of wood degrading fungus Cerrena unicolor. PLoS One 13:e0197044.  https://doi.org/10.1371/journal.pone.0197044

Nakamura S, Iwami J, Matsuda H et al (2009) Absolute stereostructures of inoterpenes A-F from sclerotia of Inonotus obliquus. Tetrahedron 65:2443–2450.

Nikolovska-Nedelkoska D, Atanasova-Pančevska N, Amedi H et al (2013) Screening of antibacterial and antifungal activities of selected Macedonian wild mushrooms. Zb Matice Srp Za Prir Nauk 124:333–340. https://doi.org/10.2298/ZMSPN1324333N DOI

Nowacka N, Nowak R, Drozd M et al (2015) Antibacterial, antiradical potential and phenolic compounds of thirty-one polish mushrooms. PLoS One 10:e0140355.  https://doi.org/10.1371/journal.pone.0140355

Ohyoshi T, Mitsugi K, Higuma T et al (2019) Concise total syntheses of phelligridins A, C, and D. RSC Adv 9:7321–7323. https://doi.org/10.1039/C8RA10346A DOI

Otaka J, Araya H (2013) Two new isodrimene sesquiterpenes from the fungal culture broth of Polyporus arcularius. Phytochem Lett 6:598–601. https://doi.org/10.1016/j.phytol.2013.07.010 DOI

Park KLJ, Jung E, Ryu J et al (2016) A study of facial wrinkles improvement effect of Veratric acid from cauliflower mushroom through photo-protective mechanisms against UVB irradiation. Arch Dermatol Res 308:183–192. https://doi.org/10.1007/s00403-016-1633-z PubMed DOI

Poliwoda A, Zielińska K, Halama M, Wieczorek PP (2014) Determination of muscimol and ibotenic acid in mushrooms of Amanitaceae by capillary electrophoresis. Electrophoresis 35:2593–2599. https://doi.org/10.1002/elps.201400104 PubMed DOI

Riss TL, Moravec RA, Niles AL et al (2016) Cell Viability Assays, Assay Guidance Manual. Eli Lilly & Company and the National Center for Advancing Translational Sciences. pp 1–25

Rossiter SE, Fletcher MH, Wuest WM (2017) Natural products as platforms to overcome antibiotic resistance. Chem Rev 117:12415–12474. https://doi.org/10.1021/acs.chemrev.7b00283 PubMed DOI PMC

Ryvarden L, Melo I (2014) Poroid fungi of Europe. Fungiflora, Oslo

Seephonkai P, Samchai S, Thongsom A et al (2011) DPPH radical scavenging activity and total phenolics of Phellinus mushroom extracts collected from northeast of Thailand. Chin J Nat Medicines 9:441–445. https://doi.org/10.3724/SP.J.1009.2011.00441 DOI

Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2(5):a000414.  https://doi.org/10.1101/cshperspect.a000414

Srinivasulu C, Ramgopal M, Ramanjaneyulu G, Anuradha CM, Suresh Kumar C (2018) Syringic acid (SA) - A Review of Its Occurrence, Biosynthesis, Pharmacological and Industrial Importance. Biomed Pharmacother 108:547–557. https://doi.org/10.1016/j.biopha.2018.09.069 PubMed DOI

Stajić M, Vukojević J, Ćilerdžić J (2019) Mushrooms as potential natural cytostatics. Int J Medicinal Mushrooms:143–168

Suabjakyong P, Saiki R, Griensven Van LJ et al (2015) Polyphenol extract from Phellinus igniarius protects against acrolein toxicity in vitro and provides protection in a mouse stroke model. PLoS One 10:e0122733. https://doi.org/10.1371/journal.pone.0122733

Suay I, Arenal F, Asensio FJ et al (2000) Screening of basidiomycetes for antimicrobial activities. Anton Leeuw Int J G 78:129–140. https://doi.org/10.1023/A:1026552024021 DOI

Sułkowska-Ziaja K, Maślanka A, Szewczyk A, Muszyńska B (2017) Physiologically active compounds in four species of Phellinus. NPC Natural Product Communications. https://doi.org/10.1177/1934578X1701200313 PubMed DOI

Sunthudlakhar P, Sithisarn P, Wannissorn B, Jarikasem S, Rojsanga P (2018) Phytochemical profiles, antioxidant and antibacterial activities of 11 Phellinus mushrooms collected in Thailand. Nat Prod J 9:144–156. https://doi.org/10.2174/2210315508666180621160917 DOI

Syafni N, Putra DP, Arbain D (2012) 3, 4-dihydroxybenzoic acid and 3, 4-dihydroxybenzaldehyde from the fern Trichomanes chinense L.: isolation, antimicrobial and antioxidant properties. Indones J Chem 12:273–278. https://doi.org/10.22146/ijc.21342

Venkateswarlu S, Ramachandra MS, Sethuramu K, Subbaraju GV (2002) Synthesis and antioxidant activity of hispolon, a yellow pigment from Inonotus hispidius. Indian J Chem 41B:875–877. https://doi.org/10.1002/chin.200233242 DOI

Wang Y, Shang XY, Wang SJ (2007) Structures, biogenesis, and biological activities of pyrano [4, 3-c] isochromen-4-one derivatives from the fungus Phellinus igniarius. J Nat Prod 70:296–299. https://doi.org/10.1021/np060476h PubMed DOI

Wangun HVK, Härtl A, Kiet TT, Hertweck C (2006) Inotilone and related phenylpropanoid polyketides from Inonotus sp. and their identification as potent COX and XO inhibitors. Org Biomol Chem 4:2545–2548. https://doi.org/10.1039/B604505G PubMed DOI

World Health Organization (2020a) Record number of countries contribute data revealing disturbing rates of antimicrobial resistance, World Health Organization. Available at: https://www.who.int/news-room/detail/01-06-2020-record-number-of-countries contribute-data-revealing-disturbing-rates-of-antimicrobial-resistance (Accessed: 3 July 2020)

World Health Organization (2020b) Lack of new antibiotics threatens global efforts to contain drug-resistant infections, World Health Organization. Available at: https://www.who.int/news-room/detail/17-01-2020-lack-of-new-antibiotics-threatens-global-efforts-to-contain-drug-resistant-infections (Accessed: 3 July 2020)

Wu CS, Lin ZM, Wang LN et al (2011) Phenolic compounds with NF-κB inhibitory effects from the fungus Phellinus baumii. Bioorg Med Chem Lett 21:3261–3267. https://doi.org/10.1016/j.bmcl.2011.04.025 PubMed DOI

Xie G, Zhou J, Yan X (2011) Encyclopedia of traditional Chinese medicines: molecular structures, pharmacological activities, natural sources and applications. volume 2 dg. https://doi.org/10.1007/978-3-642-16738-6

Zan LF, Qin JC, Zhang YM et al (2011) Antioxidant hispidin derivatives from medicinal mushroom Inonotus hispidus. Chem Pharm Bull 59:770–772. https://doi.org/10.1248/cpb.59.770 DOI