The influence of different compounds of trace elements on the biomass and synthesis of exopolysaccharides of mycelium Trametes versicolor (Polyporaceae, Polyporales)

Keywords: citrates of metals, zinc, manganese, copper, aquanotechnology, economic coefficient


This article presents the results of research on the influence of citrates of zinc, manganese and copper, obtained by the method of aquanotechnology, on a number of physiological indicators of a valuable medicinal mushroom Trametes versicolor 353. Previously we detected that these metal citrates stimulated the growth of mycelium more intensively than sulfates of the above-mentioned metals in equal concentrations. In the present research we investigated the influence of these metal citrates on the parameters of assimilation of carbon and nitrogen sources, metal ion accumulation and synthesis of exopolysaccharides. The degree of metals ions accumulation in the mycelium was studied by the  method of optical emission spectroscopy with an inductively coupled plasma. The economic coefficient of biomass synthesis and impact of nitrogen assimilation were higher on media with the metals citrate than on the medium with the sulfates of the studied metals. Thus, the highest economic coefficient of biomass synthesis (36%) was observed on the medium with copper citrate. Also, copper citrate (amongst the studied metals) increased the level of assimilation of the nitrogen source by up to 35%, versus 18% on the control medium. Quantitative analysis of trace elements in biomass showed that the mycelium accumulated an equal amount of zinc or manganese ions on both types of media (with citrate or sulfate of these metals). However, on the medium with copper citrate, mycelium of T. versicolor 353 accumulated copper ions better then on a medium with copper sulfate: 82.9 μg/g of biomass on the medium with copper sulfate versus 162.0 μg/g of biomass on the medium with copper citrate. Also the results show that a significant increase of biomass (by 79% relative to the control) on the copper citrate medium is due to a threefold reduction of the exopolysaccharides amount. This data indicates a greater biological activity of copper citrate,  relative to copper sulfate. Only zinc citrate raised both the synthesis of biomass and the synthesis of exopolysaccharides by 37% and 29% respectively ( relative to the control trial).


Al-Maali, G. A. (2015). Vplyv cytrativ metaliv, otrymanyh metodom akvananotehnologii’, na rist shtamiv likars’kyh makromicetiv Ganoderma lucidum 1900 i Trametes versicolor 353 [The influence of metal citrates obtained by aquananotechnology on growth of the strains of medical macromycetes Ganoderma lucidum 1900 and Trametes versicolor 353]. Ukrainian Botanical Journal, 72(4), 393–397 (in Ukrainian).

Al-Maali, G. A., Bisko, N. A., & Ostapchuk, A. M. (2016a). Vplyv sul’fatu ta cytratu midi na sklad biomasy likars’kogo gryba Trametes versicolor (Polyporales, Polyporaceae) [The effect of citrate and sulfate of copper on the biomass composition of the medicinal mushroom Trametes versicolor (Polyporales, Polyporaceae)] Visnyk of Dnipropetrovsk University. Biology, Ecology, 24(1), 119–123 (in Ukrainian).

Al-Maali, G. A., Bisko, N. A., & Ostapchuk, A. M. (2016b). Vplyv sul’fativ ta cytrativ metaliv na vuglevodnyj sklad biomasy likars’kogo gryba Trametes versicolor (Polyporales, Polyporaceae) [The effect of citrate and sulfate of different metals on carbohydrates composition of medicinal mushroom Trametes versicolor (Polyporales, Polyporaceae)]. Visnyk of Dnipropetrovsk University. Biology, Medicine, 7(1), 32–36 (in Ukrainian).

Aoyagi, H., Lino, Y., Takeo, T., Horii, Y., Morishita, Y., & Horiuchi, R. (2009). Effects of OK-432 (Picibanil) on the estrogen receptors of mcf-7 cells and potentiation of antiproliferative effects of tamoxifen in combination with OK-432. Oncology, 54(5), 414–423.

Arteiro, J. M. S., Martins, M. R., Salvador, C., Candeias, M. F., Karmali, A., & Caldeira, A. T. (2012). Protein-polysaccharides of Trametes versicolor: Production and biological activities. Medicinal Chemistry Research, 21(6), 937–943.

Banci, L. (Ed.). (2013). Metallomics and the cell. Metal Ions in Life Sciences. Springer, Netherlands.

Barros, A. B., Ferrão, J., & Fernandes, T. (2016). A safety assessment of Coriolus versicolor biomass as a food supplement. Food and Nutrition Research, 60(1), 29953.

Bisko, N. A., Babyckaja, V. G., & Buhalo, A. S. (2012). Byologycheskye svojstva lekarstvennyh makromycetov v kul’ture [Biological properties of medicinal macromycetes in culture] Alterpres, Kyiv (in Russian).

Bisko, N. A., Lomberg, M. L., Mytropolska, N. Y., & Mykchaylova, O. B. (2016). The IBK Mushroom culture collection. Alterpres, Kyiv (in Ukrainian).

Borysevych, V. B., Kaplunenko, V. G., & Kosinov, M. V. (2010). Nanomaterialy v biologii’. Osnovy nanoveterynarii’ [Nanomaterials in biology. Fundamentals of nanotechnology]. Avicena, Kyiv (in Ukrainian).

Broadley, M. R., White, P. J., Hammond, J. P., Zelko, I., & Lux, A. (2007). Zinc in plants. New Phytologist, 173(4), 677–702.

Chow, L. W. C., Lo, C. S. Y., Loo, W. T. Y., Hu, X., & Sham, J. S. T. (2003). Polysaccharide peptide mediates apoptosis by up-regulating p21 gene and down-regulating cyclin D1 gene. The American Journal of Chinese Medicine, 31(1), 1–9.

Chu, K. K. W., Ho, S. S. S., & Chow, A. H. L. (2002). Coriolus versicolor: A medicinal mushroom with promising immunotherapeutic values. Journal of Clinical Pharmacology, 42(9), 976–984.

Donatini, B. (2014). Control of oral human papillomavirus (HPV) by medicinal mushrooms, Trametes versicolor and Ganoderma lucidum: A preliminary clinical trial. International Journal of Medicinal Mushrooms, 16(5), 497–498.

Dudka, I. A., Vasser, S. P., & Jellanskaja, I. A. (1982). Metody jeksperimental’noj mikologii [Methods of experimental mycology] Naukova Dumka, Kyiv (in Russian).

Elisashvili, V. I., Wasser, S. P., & Kvesitadze, G. I. (2014). Physiology of biologically active metabolite production by medicinal mushrooms. Annals of Agrarian Science, 10(2), 63–67.

Fujita, H., Ogawa, K., Ikuzawa, M., Muto, S., Matsuki, M., Nakajima, S., Shimamura, M., Togawa, M., Yoshikumi, C., & Kawai, Y. (1988). Effect of PSK, a protein-bound polysaccharide from Coriolus versicolor, on drug-metabolizing enzymes in sarcoma-180 bearing and normal mice. International Journal of Immunopharmacology, 10(4), 445–450.

Hirose, K., Hakozaki, M., Kakuchi, J., Matsunaga, K., Yoshikumi, C., Takahashi, M., Tochikura, T. S., & Yamamoto, N. (1987). A biological response modifier, PSK, inhibits reverse transcriptase in vitro. Biochemical and Biophysical Research Communications, 149(2), 562–567.

Hobbs, C. (2005). Medicinal value of turkey tail fungus Trametes versicolor (L.: Fr.) Pilat (Aphyllophoromycetideae). International Journal of Medicinal Mushrooms, 7(3), 346–347.

Kaim, W., Schwederski, B., & Klein, A. (2013). Bioinorganic chemistry: Inorganic elements in the chemistry of life: An introduction and guide. John Wiley & Sons.

Kao, C., Jesuthasan, A. C., Bishop, K. S., Glucina, M. P., & Ferguson, L. R. (2013). Anti-cancer activities of Ganoderma lucidum: Active ingredients and pathways. Functional Foods in Health and Disease, 3(2), 48–65.

Klechak, I. R., Bis’ko, N. A., Mytropol’s’ka, N. J., Antonenko, L. O. (2013). Vplyv cytrativ biogennyh metaliv, otrymanyh metodom akvananotehnologij, na rist i biosyntetychnu aktyvnist’ likars’kogo gryba Trametes versicolor [Influence of citruses of biogenic metals, obtained by the method of aquanotechnology, on growth and biosynthetic activity of medicinal fungus Trametes versicolor]. Research Bulletin of NTUU Kyiv Polytechnic Institute, 3, 59–64 (in Ukrainian).

Latimer, G. W. (2012). Official methods of analysis of AOAC International. AOAC international.

Law, N. A., Caudle, M. T., & Pecoraro, V. L. (1998). Manganese redox enzymes and model systems: Properties, structures, and reactivity. Advances in Inorganic Chemistry, 305–440.

Leliebre-Lara, V., Monzote Fidalgo, L., Pferschy-Wenzig, E.-M., Kunert, O., Nogueiras Lima, C., & Bauer, R. (2016). In vitro antileishmanial activity of sterols from Trametes versicolor (Bres. Rivarden). Molecules, 21(8), 1045.

Mizuno, T. (1999). The extraction and development of antitumor-active polysaccharides from medicinal mushrooms in japan (review). International Journal of Medicinal Mushrooms, 1(1), 9–29.

Monma, Y., Kawana, T., & Shimizu, F. (1997). In vitro inactivation of herpes simplex virus by a biological response modifier, PSK. Antiviral Research, 35(3), 131–138.

Monro, J. A. (2003). Treatment of cancer with mushroom products. Archives of Environmental Health, 58(8), 533–537.

Ohmura, Y., Matsunaga, K., Motokawa, I., Sakurai, K., & Ando, T. (2003). Protective effects of a protein-bound polysaccharide, PSK, against Candida albicans infection in syngeneic tumor-bearing micevia Th1 cell functions. Cancer Biotherapy and Radiopharmaceuticals, 18(5), 769–780.

Ohmura, Y., Matsunaga, K., Motokawa, I., Sakurai, K., & Ando, T. (2001). Protective effects of a protein-bound polysaccharide, PSK, on Candida albicans infection in mice via tumor necrosis factor-α induction. International Immunopharmacology, 1(9–10), 1797–1811.

Pert, S. J. (1978). Osnovy kul’tivirovanija mikroorganizmov i kletok. [Fundamentals of cultivation of microorganisms and cells]. Nauka, Moscow (in Russian).

Rowan, N. J., Smith, J. E., & Sullivan, R. (2003). Immunomodulatory activities of mushroom glucans and polysaccharide-protein complexes in animals and humans (A review). International Journal of Medicinal Mushrooms, 5(2), 95–110.

Staats, C. C., Kmetzsch, L., Schrank, A., & Vainstein, M. H. (2013). Fungal zinc metabolism and its connections to virulence. Frontiers in Cellular and Infection Microbiology, 3, 65.

Standish, L. J., Wenner, C. A., Sweet, E. S., Bridge, C., Nelson, A., Martzen, M., Novack, J., & Torkelson, C. (2008). Trametes versicolor mushroom immune therapy in breast cancer. Journal of the Society for Integrative Oncology, 6(3), 122–128.

Titova, L. O., & Klechak, I. R. (2015). Osoblyvosti kul’tyvuvannja vyshhogo bazydial’nogo gryba Trametes zonatus na ridkyh seredovyshhah. [Features of cultivation of higher basidial fungus Trametes zonatus on liquid medium]. Naukovi Visti Nacional’nogo Tehnichnogo Universytetu Ukrai’ny Kyi’vs’kyj Politehnichnyj Instytut, 3, 76–83 (in Ukrainian).

Torkelson, C. J., Sweet, E., Martzen, M. R., Sasagawa, M., Wenner, C. A., Gay, J., Putiri, A., & Standish, L. J. (2012). Phase 1 clinical trial of Trametes versicolor in women with breast cancer. ISRN Oncology, 251632.

Tsukagoshi, S. (1984). Krestin (PSK). Cancer Treatment Reviews, 11(2), 131–155.

Wenner, C., Inatsuka, C., Davis Smith, T., Sasagawa, M., Martzen, M., Standish, L., Dasis, M., & Lu, H. (2013). Anti-tumor actions of Trametes versicolor extract polysaccharide K include activation of dendritic cells and gamma delta T cells. Planta Medica, 79(10).

Yeung, J. H. K., Chiu, L. C. M., & Ooi, V. E. C. (1995). Effect of polysaccharide peptide (PSP) on in vivo sulphation and glucuronidation of paracetamol in the rat. European Journal of Drug Metabolism and Pharmacokinetics, 20(4), 287–292.

Ying, J., Mao, X., Ma, Q., Zong, Y., & Wen, H. (1987). Icons of medicinal fungi from China (translated, Yuehan X). Science Press, Beijing.