Iron and zinc mycelial bioaccumulation in Agaricus subrufescens strains
DOI:
https://doi.org/10.5433/1679-0359.2019v40n6p2513Palabras clave:
Agaricus blazei, Agaricus brasiliensis, Iron, Metal, Mycelia, Translocation.Resumen
Agaricus subrufescens, a basidiomycete native to Brazil, is worldwide cultivated due to its medicinal properties. This fungus is capable of bioaccumulating metals in the mycelial biomass when cultured in the presence of them; however, this capacity is little explored for functional food production. This study aimed to evaluate the amount of iron or zinc bioaccumulated in the vegetative mycelium of sixteen strains of A. subrufescens. Mycelia were grown in malt extract agar added with 50 mg/L of iron or with 7.5 mg/L of zinc. The metal bioaccumulation in the mycelial biomass was strain-dependent. In general, metal can inhibit or stimulate the mycelial growth ranging from -81 to +78% for iron and from -86 to +100% for zinc. The highest bioaccumulated iron and zinc concentrations in the mycelial biomass was 2,595.65 mg/kg and 1,655.83 mg/kg, respectively and occurred in the U4-4 strain. The supplementation of mycelial biomass using iron or zinc is an alternative to develop food supplements, that can be used both in the human and animal diet and in the prevention of diseases.Citas
ALMEIDA, S. M.; UMEO, S. H.; MARCANTE, R. C.; YOKOTA, M. E.; VALLE, J. S.; DRAGUNSKI, D. C.; COLAUTO, N. B.; LINDE, G. A. Iron bioaccumulation in mycelium of Pleurotus ostreatus. Brazilian Journal of Microbiology, São Paulo, v. 46, n. 1, p. 195-200, 2015. DOI: 10.1590/S1517-838246120130695
ANDERSON, J. G.; ERIKSON, K. M. The importance of trace elements for neurological function. In: PREEDY, V.; WATSON, R.; MARTIN, C. Handbook of behavior, food and nutrition. New York: Springer, 2011. p. 423-439.
BERTÉLI, M. B. D.; UMEO, S. H.; BERTÉLI, A.; VALLE, J. S.; LINDE, G. A.; COLAUTO, N. B. Mycelial antineoplastic activity of Agaricus blazei. World Journal of Microbiology and Biotechnology, Netherlands, v. 30, n. 8, p. 2307-2313, 2014. DOI: 10.1007/s11274-014-1656-6
BHATIA, P.; PRAKASH, R.; PRAKASH, N. T. Selenium uptake by edible oyster mushrooms (Pleurotus sp.) from selenium-hyperaccumulated wheat straw. Journal of Nutritional Science and Vitaminology, Tokyo, v. 59, n. 1, p. 69-72, 2013. DOI: 10.3177/jnsv.59.69
COLAUTO, N. B.; AIZONO, P. A. M. C. M.; RIBEIRO, L.; PACCOLA-MEIRELLES, L. D.; LINDE, G. A. Temperature and pH conditions for mycelial growth of Agaricus brasiliensis on axenic cultivation. Semina: Ciências Agrárias, Londrina, v. 29, n. 2, p. 307-312, 2008.
COLAUTO, N. B.; SILVEIRA, A. R. D.; EIRA, A. F. D.; LINDE, G. A. Alternative to peat for Agaricus brasiliensis yield. Bioresource Technology, Miramar, v. 101, n. 2, p. 712-716, 2010. DOI: 10.1016/j.biortech.2009.08.052
DUNN, L. L.; RAHMANTO, Y. S.; RICHARDSON, D. R. Iron uptake and metabolism in the new millennium. Trends in Cell Biology, Amsterdam, v. 17, n. 2, p. 93-100, 2007. DOI: 10.1016/j.tcb.2006.12.003
FOOD AND AGRICULTURE ORGANIZATION – FAO. Guidelines on food fortification with micronutrients. World Health Organization, Food and Agricultural Organization of the United Nations. Genebra: WHO, 2006.
GADD, G. M. Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycological Research, Cambridge, v. 111, n. 1, p. 3-49, 2007. DOI: 10.1016/j.mycres.2006.12.001
HAAS, H. Molecular genetics of fungal siderophore biosynthesis and uptake: the role of siderophores in iron uptake and storage. Applied Microbiology and Biotechnology, Berlin, v. 62, n. 4, p. 316-330, 2003. DOI: 10.1007/s00253-003-1335-2
KAWAGISHI, H.; INAGAKI, R.; KANAO, T.; MIZUNO, T. Fractionation and antitumor activity of the water-in-soluble residue of Agaricus blazei fruiting bodies. Carbohydrate Research, Amsterdam, v. 186, n. 2, p. 267-273, 1989. DOI: 10.1016/0008-6215(89)84040-6
LEE, B. C.; BAE, J. T.; PYO, H. B.; CHOE, T. B.; KIM, S. W.; HWANG, H.J.; YUN, J. W. Submerged culture conditions for the production of mycelial biomass and exopolysaccharides by the edible Basidiomycete Grifola frondosa. Enzyme and Microbial Technology, Amsterdam, v. 35, n. 5, p. 369-376, 2004. DOI: 10.1016/j.enzmictec.2003.12.015
MANTOVANI, T. R. D. A.; TANAKA, H. S.; UMEO, S. H.; ZAGHI-JUNIOR, L. L.; VALLE, J. S.; PACCOLA-MEIRELLES, L. D.; LINDE, G. A.; COLAUTO, N. B. Cryopreservation at -20 and -70 °C of Pleurotus ostreatus on grains. Indian Journal of Microbiology, v. 52, n. 3, p. 484-488, 2012. DOI: 10.1016/j.enzmictec.2003.12.015
MARCANTE, R. D. C.; MENIQUETTI, A.; PASCOTTO, C. R.; GAZIN, Z. C.; MAGALHÃES, H. M.; COLAUTO, N. B.; LINDE. G. A. Bioacumulação de zinco em micélio de Agaricus subrufescens. Arquivos de Ciências Veterinárias e Zoologia da UNIPAR, Umuarama, v. 17, n. 4, p. 249-252, 2014. DOI: 10.1016/j.enzmictec.2003.12.015
MIZUNO, T. Kawariharatake, Agaricus blazei Murill: medicinal and dietary effects. Food Reviews International, New York, v. 11, n. 1, p. 167-172, 1995. DOI: 10.1080/87559129509541026
MOURÃO, F.; LINDE, G. A.; MESSA, V.; CUNHA JÚNIOR, P. L.; SILVA, A. V.; EIRA, A. F.; COLAUTO, N. B. Antineoplasic activity of Agaricus brasiliensis basidiocarps on different maturation phases. Brazilian Journal of Microbiology, São Paulo, v. 40, n. 4, p. 901-905, 2009. DOI: 10.1590/S1517-83822009000400022
MOURÃO, F.; UMEO, S. H.; BERTÉLI, M. B. D.; LOURENÇO, E. L.; GASPAROTTO JUNIOR, A.; TAKEMURA, O. S.; LINDE, G. A.; COLAUTO, N. B. Anti-inflammatory activity of Agaricus blazei in different basidiocarp maturation phases. Food and Agricultural Immunology, United Kingdom, v. 22, n. 4, p. 325-333, 2011a. DOI: 10.1080/09540105.2011.581272
MOURÃO, F.; UMEO, S. H.; TAKEMURA, O. S.; LINDE, G. A.; COLAUTO, N. B. Antioxidant activity of Agaricus brasiliensis basidiocarps on different maturation phases. Brazilian Journal of Microbiology, São Paulo, v. 42, n. 1, p. 197-202, 2011b. DOI: 10.1590/S1517-83822011000100024
MSHANDETE, A. M.; MGONJA, J. R. Submerged liquid fermentation of some Tanzanian basidiomycetes for the production of mycelial biomass, exopolysaccharides and mycelium protein using wastes peels media. ARPN Journal of Agricultural and Biological Science, Chak Shahzad Islamabad, v. 4, n. 6, p. 1-13, 2009.
PERES, P. M.; KOURY, J. C. Zinco, imunidade, nutrição e exercício. Ceres: Nutrição e Saúde, v. 1, n. 1, p. 9-18, 2006.
PHILPOTT, C. C. Iron uptake in fungi: a system for every source. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Amsterdam, v. 1763, n. 7, p. 636-645, 2006. DOI: 10.1016/j.bbamcr.2006.05.008
PONTECORVO, G.; ROPER, J. A.; CHEMMONS, L. M.; MACDONALD K. D., BUFTON, A. W. J. The Genetics of Aspergillus nidulans. Advances in Genetics, Amsterdam, v. 5, p. 141-238, 1953. 10.1016/S0065-2660(08)60408-3
SANDSTEAD, H. H.; FREDERICKSON, C. J.; PENLAND, J. G. History of zinc as related to brain function. The Journal of Nutrition, Bethesda, v. 130, n. 2S, p. 496S-502S, 2000. DOI: 10.1093/jn/130.2.496S
UMEO, S. H; SOUZA, G. P. N.; RAPACHI, P. M.; GARCIA, L. D.; PACCOLA-MEIRELLES, L. D.; VALLE, J. S.; COLAUTO, N. B.; LINDE, G. A. Screening of basidiomycetes in submerged cultivation based on antioxidant activity. Genetics and Molecular Research, Ribeirão Preto, v. 14, n. 3, p. 9907-9914, 2015. DOI: 10.4238/2015.August.19.25
VIEIRA, P. A. F.; GONTIJO, D. C.; VIEIRA, B. C.; FONTES, E.A.F.; ASSUNÇÃO, L. S.; LEITE, J. P. V.; OLIVEIRA, M. G. A.; KASUYA, M. C. M. Antioxidant activities, total phenolics and metal contents in Pleurotus ostreatus mushrooms enriched with iron, zinc or lithium. LWT - Food Science and Technology, Amsterdam, v. 54, n. 2, p. 421-425, 2013. DOI: 10.1016/j.lwt.2013.06.016
WISITRASSAMEEWONG, K.; KARUNARATHNA, S. C.; THONGKLANG, N.; ZHAO, R.; CALLAC, P.; MOUKHA, S.; FERANDON, C.; CHUKEATIROTE, E.; HYDE, K.D. Agaricus subrufescens: a review. Saudi Journal of Biological Sciences, Chiang Rai, v. 19, n. 2, p. 131-146, 2012. DOI: 10.1016/j.sjbs.2012.01.003
WORLD HEALTH ORGANIZATION - WHO. Iron deficiency anaemia: assessment, prevention and control: a guide for programme managers. Geneva: World Health Organization, 2001.
YOKOTA, M.; FRISON, P.; MARCANTE, R.; JORGE, L. F.; VALLE, J. S.; DRAGUNSKI, D. C.; COLAUTO, N. B.; LINDE, G. A. Iron translocation in Pleurotus ostreatus basidiocarps: production, bioavailability, and antioxidant activity. Genetics and Molecular Research, Ribeirão Preto, v. 15, n. 1, p. 1-10, 2016.
ANDERSON, J. G.; ERIKSON, K. M. The importance of trace elements for neurological function. In: PREEDY, V.; WATSON, R.; MARTIN, C. Handbook of behavior, food and nutrition. New York: Springer, 2011. p. 423-439.
BERTÉLI, M. B. D.; UMEO, S. H.; BERTÉLI, A.; VALLE, J. S.; LINDE, G. A.; COLAUTO, N. B. Mycelial antineoplastic activity of Agaricus blazei. World Journal of Microbiology and Biotechnology, Netherlands, v. 30, n. 8, p. 2307-2313, 2014. DOI: 10.1007/s11274-014-1656-6
BHATIA, P.; PRAKASH, R.; PRAKASH, N. T. Selenium uptake by edible oyster mushrooms (Pleurotus sp.) from selenium-hyperaccumulated wheat straw. Journal of Nutritional Science and Vitaminology, Tokyo, v. 59, n. 1, p. 69-72, 2013. DOI: 10.3177/jnsv.59.69
COLAUTO, N. B.; AIZONO, P. A. M. C. M.; RIBEIRO, L.; PACCOLA-MEIRELLES, L. D.; LINDE, G. A. Temperature and pH conditions for mycelial growth of Agaricus brasiliensis on axenic cultivation. Semina: Ciências Agrárias, Londrina, v. 29, n. 2, p. 307-312, 2008.
COLAUTO, N. B.; SILVEIRA, A. R. D.; EIRA, A. F. D.; LINDE, G. A. Alternative to peat for Agaricus brasiliensis yield. Bioresource Technology, Miramar, v. 101, n. 2, p. 712-716, 2010. DOI: 10.1016/j.biortech.2009.08.052
DUNN, L. L.; RAHMANTO, Y. S.; RICHARDSON, D. R. Iron uptake and metabolism in the new millennium. Trends in Cell Biology, Amsterdam, v. 17, n. 2, p. 93-100, 2007. DOI: 10.1016/j.tcb.2006.12.003
FOOD AND AGRICULTURE ORGANIZATION – FAO. Guidelines on food fortification with micronutrients. World Health Organization, Food and Agricultural Organization of the United Nations. Genebra: WHO, 2006.
GADD, G. M. Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycological Research, Cambridge, v. 111, n. 1, p. 3-49, 2007. DOI: 10.1016/j.mycres.2006.12.001
HAAS, H. Molecular genetics of fungal siderophore biosynthesis and uptake: the role of siderophores in iron uptake and storage. Applied Microbiology and Biotechnology, Berlin, v. 62, n. 4, p. 316-330, 2003. DOI: 10.1007/s00253-003-1335-2
KAWAGISHI, H.; INAGAKI, R.; KANAO, T.; MIZUNO, T. Fractionation and antitumor activity of the water-in-soluble residue of Agaricus blazei fruiting bodies. Carbohydrate Research, Amsterdam, v. 186, n. 2, p. 267-273, 1989. DOI: 10.1016/0008-6215(89)84040-6
LEE, B. C.; BAE, J. T.; PYO, H. B.; CHOE, T. B.; KIM, S. W.; HWANG, H.J.; YUN, J. W. Submerged culture conditions for the production of mycelial biomass and exopolysaccharides by the edible Basidiomycete Grifola frondosa. Enzyme and Microbial Technology, Amsterdam, v. 35, n. 5, p. 369-376, 2004. DOI: 10.1016/j.enzmictec.2003.12.015
MANTOVANI, T. R. D. A.; TANAKA, H. S.; UMEO, S. H.; ZAGHI-JUNIOR, L. L.; VALLE, J. S.; PACCOLA-MEIRELLES, L. D.; LINDE, G. A.; COLAUTO, N. B. Cryopreservation at -20 and -70 °C of Pleurotus ostreatus on grains. Indian Journal of Microbiology, v. 52, n. 3, p. 484-488, 2012. DOI: 10.1016/j.enzmictec.2003.12.015
MARCANTE, R. D. C.; MENIQUETTI, A.; PASCOTTO, C. R.; GAZIN, Z. C.; MAGALHÃES, H. M.; COLAUTO, N. B.; LINDE. G. A. Bioacumulação de zinco em micélio de Agaricus subrufescens. Arquivos de Ciências Veterinárias e Zoologia da UNIPAR, Umuarama, v. 17, n. 4, p. 249-252, 2014. DOI: 10.1016/j.enzmictec.2003.12.015
MIZUNO, T. Kawariharatake, Agaricus blazei Murill: medicinal and dietary effects. Food Reviews International, New York, v. 11, n. 1, p. 167-172, 1995. DOI: 10.1080/87559129509541026
MOURÃO, F.; LINDE, G. A.; MESSA, V.; CUNHA JÚNIOR, P. L.; SILVA, A. V.; EIRA, A. F.; COLAUTO, N. B. Antineoplasic activity of Agaricus brasiliensis basidiocarps on different maturation phases. Brazilian Journal of Microbiology, São Paulo, v. 40, n. 4, p. 901-905, 2009. DOI: 10.1590/S1517-83822009000400022
MOURÃO, F.; UMEO, S. H.; BERTÉLI, M. B. D.; LOURENÇO, E. L.; GASPAROTTO JUNIOR, A.; TAKEMURA, O. S.; LINDE, G. A.; COLAUTO, N. B. Anti-inflammatory activity of Agaricus blazei in different basidiocarp maturation phases. Food and Agricultural Immunology, United Kingdom, v. 22, n. 4, p. 325-333, 2011a. DOI: 10.1080/09540105.2011.581272
MOURÃO, F.; UMEO, S. H.; TAKEMURA, O. S.; LINDE, G. A.; COLAUTO, N. B. Antioxidant activity of Agaricus brasiliensis basidiocarps on different maturation phases. Brazilian Journal of Microbiology, São Paulo, v. 42, n. 1, p. 197-202, 2011b. DOI: 10.1590/S1517-83822011000100024
MSHANDETE, A. M.; MGONJA, J. R. Submerged liquid fermentation of some Tanzanian basidiomycetes for the production of mycelial biomass, exopolysaccharides and mycelium protein using wastes peels media. ARPN Journal of Agricultural and Biological Science, Chak Shahzad Islamabad, v. 4, n. 6, p. 1-13, 2009.
PERES, P. M.; KOURY, J. C. Zinco, imunidade, nutrição e exercício. Ceres: Nutrição e Saúde, v. 1, n. 1, p. 9-18, 2006.
PHILPOTT, C. C. Iron uptake in fungi: a system for every source. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Amsterdam, v. 1763, n. 7, p. 636-645, 2006. DOI: 10.1016/j.bbamcr.2006.05.008
PONTECORVO, G.; ROPER, J. A.; CHEMMONS, L. M.; MACDONALD K. D., BUFTON, A. W. J. The Genetics of Aspergillus nidulans. Advances in Genetics, Amsterdam, v. 5, p. 141-238, 1953. 10.1016/S0065-2660(08)60408-3
SANDSTEAD, H. H.; FREDERICKSON, C. J.; PENLAND, J. G. History of zinc as related to brain function. The Journal of Nutrition, Bethesda, v. 130, n. 2S, p. 496S-502S, 2000. DOI: 10.1093/jn/130.2.496S
UMEO, S. H; SOUZA, G. P. N.; RAPACHI, P. M.; GARCIA, L. D.; PACCOLA-MEIRELLES, L. D.; VALLE, J. S.; COLAUTO, N. B.; LINDE, G. A. Screening of basidiomycetes in submerged cultivation based on antioxidant activity. Genetics and Molecular Research, Ribeirão Preto, v. 14, n. 3, p. 9907-9914, 2015. DOI: 10.4238/2015.August.19.25
VIEIRA, P. A. F.; GONTIJO, D. C.; VIEIRA, B. C.; FONTES, E.A.F.; ASSUNÇÃO, L. S.; LEITE, J. P. V.; OLIVEIRA, M. G. A.; KASUYA, M. C. M. Antioxidant activities, total phenolics and metal contents in Pleurotus ostreatus mushrooms enriched with iron, zinc or lithium. LWT - Food Science and Technology, Amsterdam, v. 54, n. 2, p. 421-425, 2013. DOI: 10.1016/j.lwt.2013.06.016
WISITRASSAMEEWONG, K.; KARUNARATHNA, S. C.; THONGKLANG, N.; ZHAO, R.; CALLAC, P.; MOUKHA, S.; FERANDON, C.; CHUKEATIROTE, E.; HYDE, K.D. Agaricus subrufescens: a review. Saudi Journal of Biological Sciences, Chiang Rai, v. 19, n. 2, p. 131-146, 2012. DOI: 10.1016/j.sjbs.2012.01.003
WORLD HEALTH ORGANIZATION - WHO. Iron deficiency anaemia: assessment, prevention and control: a guide for programme managers. Geneva: World Health Organization, 2001.
YOKOTA, M.; FRISON, P.; MARCANTE, R.; JORGE, L. F.; VALLE, J. S.; DRAGUNSKI, D. C.; COLAUTO, N. B.; LINDE, G. A. Iron translocation in Pleurotus ostreatus basidiocarps: production, bioavailability, and antioxidant activity. Genetics and Molecular Research, Ribeirão Preto, v. 15, n. 1, p. 1-10, 2016.
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2019-08-29
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Umeo, S. H., Faria, M. G. I., Vilande, S. S. S., Dragunski, D. C., Valle, J. S. do, Colauto, N. B., & Linde, G. A. (2019). Iron and zinc mycelial bioaccumulation in Agaricus subrufescens strains. Semina: Ciências Agrárias, 40(6), 2513–2522. https://doi.org/10.5433/1679-0359.2019v40n6p2513
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