Food Science and Biotechnology

, Volume 26, Issue 1, pp 159–165 | Cite as

Antifungal-demelanizing properties and RAW264.7 macrophages stimulation of glucan sulfate from the mycelium of the mushroom Ganoderma lucidum

  • Wan Abd Al Qadr Imad Wan-Mohtar
  • Christina Viegelmann
  • Anita Klaus
  • Sarina Abdul Halim Lim


Underutilized mycelium of Ganoderma lucidum BCCM 31549 has been a significant source of a glucan sulfate (GS) possessing therapeutic activities. GS have been evaluated for their antifungaldemelanizing properties and nitrite oxide production from stimulated RAW264.7 macrophages. GS exhibited antifungal activity against Aspergillus niger A60 with a minimum inhibitory concentration of 60 mg/mL and a minimum fungicidal concentration of 100 mg/mL. At 60mg/mL (sublethal) and 30mg/mL (subinhibitory) doses of GS, the mycelium of A. niger A60 was successfully demelanized with a conidiophore head and black pigment reduction. Additionally, GS successfully stimulated RAW264.7 macrophage cells at a concentration of 500 μg/mL to produce 0.45 μM of nitric oxide. The GS-stimulated RAW264.7 macrophages were morphologically similar to those treated with lipopolysaccharide. The results highlight a novel bifunctional property of mycelial GS from G. lucidum.


antifungal activity demelanization Ganoderma lucidum glucan sulfate nitric oxide production 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Ferreira IC, Heleno SA, Reis FS, Stojkovic D, Queiroz MJ, Vasconcelos MH, Sokovic M. Chemical features of Ganoderma polysaccharides with antioxidant, antitumor and antimicrobial activities. Phytochemistry 114: 38–55 (2015)CrossRefGoogle Scholar
  2. 2.
    Klaus A, Kozarski M, Vunduk J, Todorovic N, Jakovljevic D, Zizak Z, Pavlovic V, Levic S, Niksic M, Van Griensven LJ. Biological potential of extracts of the wild edible basidiomycete mushroom Grifola frondosa. Food. Res. Int. 67: 272–283 (2015)CrossRefGoogle Scholar
  3. 3.
    Fazenda ML, Seviour R, McNeil B, Harvey LM. Submerged culture fermentation of “higher fungi”: the macrofungi. Adv. Appl. Microbiol. 63: 33–103 (2008)CrossRefGoogle Scholar
  4. 4.
    Wan-Mohtar WAAQI, Young L, Abbott GM, Clements C, Harvey LM, McNeil B. Antimicrobial properties and cytotoxicity of sulfated (1,3)-beta-D-glucan from the mycelium of the mushroom Ganoderma lucidum. J. Microbiol. Biotechn. 26: 999–1010 (2016)CrossRefGoogle Scholar
  5. 5.
    Kozarski M, Klaus A, Niksic M, Jakovljevic D, Helsper JPFG, Van Griensven LJLD. Antioxidative and immunomodulating activities of polysaccharide extracts of the medicinal mushrooms Agaricus bisporus, Agaricus brasiliensis, Ganoderma lucidum and Phellinus linteus. Food Chem. 129: 1667–1675 (2011)CrossRefGoogle Scholar
  6. 6.
    Wang H, Ng TB. Ganodermin, an antifungal protein from fruiting bodies of the medicinal mushroom Ganoderma lucidum. Peptides 27: 27–30 (2006)CrossRefGoogle Scholar
  7. 7.
    Heleno SA, Ferreira IC, Esteves AP, Ciric A, Glamoclija J, Martins A, Sokovic M, Queiroz MJR. Antimicrobial and demelanizing activity of Ganoderma lucidum extract, p-hydroxybenzoic and cinnamic acids and their synthetic acetylated glucuronide methyl esters. Food. Chem. Toxicol. 58: 95–100 (2013)CrossRefGoogle Scholar
  8. 8.
    Tung NT, Cuong TD, Hung TM, Lee JH, Woo MH, Choi JS, Kim J, Ryu SH, Min BS. Inhibitory effect on NO production of triterpenes from the fruiting bodies of Ganoderma lucidum. Bioorg. Med. Chem. Lett. 23: 1428–1432 (2013)CrossRefGoogle Scholar
  9. 9.
    Wan Mohtar WAAQI, Latif NA, Harvey LM, McNeil B. Production of exopolysaccharide by Ganoderma lucidum in a repeated-batch fermentation. Biocatal. Agric. Biotechnol. 6: 91–101 (2016)Google Scholar
  10. 10.
    Wan-Mohtar WAAQI, Ab Kadir S, Saari N. The morphology of Ganoderma lucidum mycelium in a repeated-batch fermentation for exopolysaccharide production. Biotechnol. Rep. 11: 2–11 (2016)CrossRefGoogle Scholar
  11. 11.
    Wan-Mohtar WAAQI, Malek RA, Harvey LM, McNeil B. Exopolysaccharide production by Ganoderma lucidum immobilised on polyurethane foam in a repeated-batch fermentation. Biocatal. Agric. Biotechnol. 8: 24–31 (2016)Google Scholar
  12. 12.
    Zhao W, Xu JW, Zhong JJ. Enhanced production of ganoderic acids in static liquid culture of Ganoderma lucidum under nitrogen-limiting conditions. Bioresource Technol. 102: 8185–8190 (2011)CrossRefGoogle Scholar
  13. 13.
    Hsieh C, Tseng M-H, Liu C-J. Production of polysaccharides from Ganoderma lucidum (CCRC 36041) under limitations of nutrients. Enzyme Microb. Tech. 38: 109–117 (2006)CrossRefGoogle Scholar
  14. 14.
    Wang J, Zhang L. Structure and chain conformation of five water-soluble derivatives of a ß-D-glucan isolated from Ganoderma lucidum. Carbohyd. Res. 344: 105–112 (2009)CrossRefGoogle Scholar
  15. 15.
    Karnjanapratum S, Tabarsa M, Cho M, You S. Characterization and immunomodulatory activities of sulfated polysaccharides from Capsosiphon fulvescens. Int. J. Biol. Macromol. 51: 720–729 (2012)CrossRefGoogle Scholar
  16. 16.
    Liao SF, Liang CH, Ho MY, Hsu TL, Tsai TI, Hsieh YS, Tsai CM, Li ST, Cheng YY, Tsao SM, Lin TY, Lin ZY, Yang WB, Ren CT, Lin KI, Khoo KH, Lin CH, Hsu HY, Wu CY, Wong CH. Immunization of fucose-containing polysaccharides from Reishi mushroom induces antibodies to tumor-associated Globo H-series epitopes. P. Natl. Acad. Sci. USA 110: 13809–13814 (2013)CrossRefGoogle Scholar
  17. 17.
    Llaurado G, Morris HJ, Ferrera L, Camacho M, Castan L, Lebeque Y, Beltran Y, Cos P, Bermudez RC. In-vitro antimicrobial activity and complement/macrophage stimulating effects of a hot-water extract from mycelium of the oyster mushroom Pleurotus sp. Innov. Food. Sci. Emerg. 30: 177–183 (2015)CrossRefGoogle Scholar
  18. 18.
    Nayak A, Nayak RN, Bhat K. Antifungal activity of a toothpaste containing Ganoderma lucidum against Candida albicans-an in vitro study. J. Int. Oral Health 2: 51–57 (2010)Google Scholar
  19. 19.
    Liu Y, Zhang J, Tang Q, Yang Y, Guo Q, Wang Q, Wu D, Cui SW. Physicochemical characterization of a high molecular weight bioactive beta-D-glucan from the fruiting bodies of Ganoderma lucidum. Carbohyd. Polym. 101: 968–974 (2014)CrossRefGoogle Scholar
  20. 20.
    Chiong HS, Yong YK, Ahmad Z, Sulaiman MR, Zakaria ZA, Yuen KH, Hakim MN. Cytoprotective and enhanced anti-inflammatory activities of liposomal piroxicam formulation in lipopolysaccharide-stimulated RAW 264.7 macrophages. Int. J. Nanomed. 8: 1245 (2013)Google Scholar
  21. 21.
    Ji Z, Tang Q, Zhang J, Yang Y, Jia W, Pan Y. Immunomodulation of RAW264. 7 macrophages by GLIS, a proteopolysaccharide from Ganoderma lucidum. J. Ethnopharmacol. 112: 445–450 (2007)Google Scholar
  22. 22.
    Smania EF, Delle Monache F, Smania A, Yunes RA, Cuneo RS. Antifungal activity of sterols and triterpenes isolated from Ganoderma annulare. Fitoterapia 74: 375–377 (2003)CrossRefGoogle Scholar
  23. 23.
    Bromuro C, Romano M, Chiani P, Berti F, Tontini M, Proietti D, Mori E, Torosantucci A, Costantino P, Rappuoli R. Beta-glucan-CRM197 conjugates as candidates antifungal vaccines. Vaccine 28: 2615–2623 (2010)CrossRefGoogle Scholar
  24. 24.
    Gomez BL, Nosanchuk JD. Melanin and fungi. Curr. Opin. Infect. Dis. 16: 91–96 (2003)CrossRefGoogle Scholar
  25. 25.
    Rosa LH, Almeida Vieira Mde L, Santiago IF, Rosa CA. Endophytic fungi community associated with the dicotyledonous plant Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae) in Antarctica. FEMS Microbiol. Ecol. 73: 178–189 (2010)Google Scholar
  26. 26.
    Brakhage A, Liebmann B. Aspergillus fumigatus conidial pigment and cAMP signal transduction: Significance for virulence. Med. Mycol. 43: 75–82 (2005)CrossRefGoogle Scholar
  27. 27.
    Fagade O, Oyelade A. A comparative study of the antibacterial activities of some wood-decay fungi to synthetic antibiotic discs. Electron. J. Environ. Agr. Food. Chem. 8: 184–188 (2009)Google Scholar
  28. 28.
    Droge W. Free radicals in the physiological control of cell function. Physiol. Rev. 82: 47–95 (2002)CrossRefGoogle Scholar
  29. 29.
    Mills CD, Kincaid K, Alt JM, Heilman MJ, Hill AM. M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 164: 6166–6173 (2000)CrossRefGoogle Scholar
  30. 30.
    Shi M, Zhang Z, Yang Y. Antioxidant and immunoregulatory activity of Ganoderma lucidum polysaccharide (GLP). Carbohyd. Polym. 95: 200–206 (2013)CrossRefGoogle Scholar
  31. 31.
    Shi M, Yang Y, Guan D, Wang Y, Zhang Z. Evaluation of solid-state fermentation by Ganoderma lucidum using soybean curd residue. Food Bioprocess Tech. 6: 1856–1867 (2013)CrossRefGoogle Scholar
  32. 32.
    Datta C, Das D, Mondal P, Chakraborty B, Sengupta M, Bhattacharjee CR. Novel water soluble neutral vanadium (IV)–antibiotic complex: Antioxidant, immunomodulatory and molecular docking studies. Eur. J. Med. Chem. 97: 214–224 (2015)CrossRefGoogle Scholar
  33. 33.
    Labro M-T. Immunomodulatory effects of antimicrobial agents. part I: antibacterial and antiviral agents. Expert Rev. Anti-Infe. 10: 319–340 (2012)Google Scholar
  34. 34.
    Allison RD, Tong X, Moorman AC, Ly KN, Rupp L, Xu F, Gordon SC, Holmberg SD, Investigators CHCS. Increased incidence of cancer and cancer-related mortality among persons with chronic Hepatitis C infection, 2006-2010. J. Hepatol. 63: 822–828 (2015)CrossRefGoogle Scholar
  35. 35.
    Lindequist U, Niedermeyer TH, Julich WD. The pharmacological potential of mushrooms. Evid-Based Compl. Alt. 2: 285–299 (2005)CrossRefGoogle Scholar

Copyright information

© The Korean Society of Food Science and Technology and Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Wan Abd Al Qadr Imad Wan-Mohtar
    • 1
    • 2
    • 5
  • Christina Viegelmann
    • 2
  • Anita Klaus
    • 3
  • Sarina Abdul Halim Lim
    • 4
  1. 1.Institute of Biological Sciences, Faculty of ScienceUniversity of MalayaKuala LumpurMalaysia
  2. 2.Fermentation Centre, Strathclyde Institute of Pharmacy and Biomedical SciencesUniversity of StrathclydeGlasgow, ScotlandUK
  3. 3.Institute for Food Technology and BiochemistryUniversity of Belgrade - Faculty of AgricultureBelgradeSerbia
  4. 4.Department of Food TechnologyFaculty of Food Science and Technology Universiti Putra MalaysiaSerdangMalaysia
  5. 5.Mushroom Research CentreUniversity of MalayaKuala LumpurMalaysia

Personalised recommendations