Use of spent mushroom substrate (SMS) in new production cycles and evaluation of the antioxidant activity of Lentinus crinitus and Pleurotus spp.

Authors

  • Olavo Bilac Quaresma de Oliveira Filho Universidade do Estado do Amapá https://orcid.org/0000-0001-7259-2066
  • Miria Benetati Delgado Bertéli Universidade Estadual de Maringá, Brasil
  • Nelson Barros Colauto Universidade Tecnológica Federal do Paraná, Brasil
  • Giani Andrea Linde Colauto Centro Universitário Unifatecie, Brasil
  • Perseu da Silva Aparicio Universidade do Estado do Amapá, Brasil
  • William Kalhy Silva Xavier Universidade do Estado do Amapá, Brasil
  • Carlos Henrique Medeiros de Abreu Universidade do Estado do Amapá, Brasil
  • Juliana Silveira do Valle Universidade Paranaense, Brasil

DOI:

https://doi.org/10.66104/m58yet98

Keywords:

Antioxidant; basidiomycete; microbial succession; waste valorization.

Abstract

Lentinus crinitus and Pleurotus spp. are mushrooms that can be produced in lignocellulosic agro-industrial by-products. After mushroom production, the substrate containing the mycelium constitutes the spent mushroom substrate (SMS). Its reuse in new production cycles generates prospects for a more efficient production chain. The SMS from L. crinitus was used to produce Pleurotus spp. and and the reverse path was taken, to verify the possibility of SMS reuse. The antioxidant activity of the SMS generated in the two cycles of cultivation and the mushrooms harvested was evaluated. Cultivation in SMS decreased productivity, biological efficiency, and substrate consumption. P. djamor and P. ostreatus produced in SMS from L. crinitus showed a reduction in productivity of 4.4 and 4.2 times, respectively. Biological efficiency followed the same decreasing trend. The microbial succession reduced the SMS antioxidant activity by the FRAP (ferric reducing antioxidant power) and BCLA (beta-carotene/linoleic acid co-oxidation system) methods. Only the antioxidant activity by the DPPH (2,2-diphenyl-1-picrylhydrazyl) radical scavenging method of SMS increased after the second cultivation cycle. Mushrooms produced in secondary cultivation have higher DPPH antioxidant activity than in primary cultivation. L. crinitus produced in succession to P. djamor presented a 2.5-fold reduction in inhibitory concentration (IC50) compared to mushrooms from the primary cultivation. The growth in SMS also increased mushroom FRAP activity. L. crinitus grown in SMS of P. djamor, and SMS of P. ostreatus showed the highest antioxidant activities by FRAP, seven times and 6.3 times superior to reference control. Only the antioxidant activity by BCLA of P. ostreatus mushrooms grown in SMS of L. crinitus was significantly higher than the mushrooms from primary cultivation. Despite the reduction in productivity, the use of SMS in a new substrate composition increased the antioxidant activity of mushrooms. The SMS produce basidiocarps with higher content of compounds with antioxidant activity.

Downloads

Download data is not yet available.

References

Almeida, A.C.P.S., Cristo, C.C.N., Guedes-Celestino, E.L.F., Costa, J.H.Q., Silva, J.M., Silva, L.M.M.M., Santos, T.M.C., Montaldo, Y.M., 2019. Axenic cultivation of edible mushrooms in substrates developed with agroindustrials residues, in: Santos, C.C. (Ed.), Agroecology: discussion about sustainability. Atena Publisher, Paraná, pp. 89-98. https://doi.org/10.22533/at.ed.99319240710 DOI: https://doi.org/10.22533/at.ed.99319240710

Andrews, A., Singh, S., Ishani, Chandhrapati, A.; Kumar, Y.V., 2021. Utilization of spent mushroom substrate: A review. Pharma Innovation 10, 1017-1021.

Bertéli, M.B.D., Oliveira Filho, O.B.Q., Freitas, J.D.S., Bortolucci, W.C., Silva, G.R., Gazim, Z.C., Lívero, F.A.R., Lovato, E.C.W., Valle, J.S., Linde, G.A., Barros, L., Reis, F.S., Ferreira I.C.F.R., Paccola-Meirelles, L.D., Colauto, N.B., 2021a. Lentinus crinitus basidiocarp stipe and pileus: chemical composition, cytotoxicity and antioxidant activity. Eur. Food Res. Technol. 247, 1355–1366. https://doi.org/10.1007/s00217-021-03713-1 DOI: https://doi.org/10.1007/s00217-021-03713-1

Bertéli, M.B.D., Barros, L., Reis, F.S., Ferreira I.C.F.R., Glamoclija, J., Sokovic, M., Valle, J.S., Linde, G.A., Ruiz, S.P., Colauto, N.B., 2021b. Antimicrobial activity, chemical composition and cytotoxicity of Lentinus crinitus basidiocarp. Food Funct. 12, 6780-6792. https://doi.org/10.1039/D1FO00656H DOI: https://doi.org/10.1039/D1FO00656H

Bononi, V. L., Capelari, M., Maziero, R., 1995. Cultivation of Edible Mushrooms, first ed. Ícone, São Paulo.

Boonsong, S., Klaypradit, W., Wilaipun, P., 2016. Antioxidant activities of extracts from five edible mushrooms using different extractants. Agric. Nat. Resour., 50, 89-97. https://doi.org/10.1016/j.anres.2015.07.002 DOI: https://doi.org/10.1016/j.anres.2015.07.002

Braga, G.C., Eira, A.F., Celso, P.G., Colauto, N.B., 1998. Cultivation manual of Agaricus blazei Murr. ‘Cogumelo-do-Sol’, first ed. FEPAF, Botucatu.

Buendía, M.R.P., Pardo-Giménez, A., Valero, J.A.J., 2017. Spent substrates in new cultivation cycles of Pleurotus ostreatus. Sydowia 69, 73–79. http://dx.doi.org/10.12905/0380.sydowia69-2017-0073

Castro, A.L.A., Paiva, P.C.A., Banys, V.L., Dias, E.S., Santos, J., 2007. Evaluation of the production of Pleurotus sajor-caju in cotton textile mill waste, Ciênc. agrotec. 31, 1286-1290. http://dx.doi.org/10.1590/S1413-70542007000500002 DOI: https://doi.org/10.1590/S1413-70542007000500002

China Edible Fungus Association CN, 2018. The survey results for the edible fungus 2018 annual analysis of China Edible Fungus Association. http://bigdata.cefa.org.cn/output.html (accessed 09 october 2021).

Chang, S.T., Miles, P.G., 2004. Mushrooms: cultivation, nutritional value, medicinal effect, and environmental impact, second ed. CRC Press, United States.

Companhia Nacional de Abastecimento BR, 2021a. Monitoring of the Brazilian sugarcane crop 2020/21. https://www.conab.gov.br/info-agro/safras/cana (accessed 26 may 2021).

Companhia Nacional de Abastecimento BR, 2021b. Monitoring of the Brazilian soybean crop 2020/21. https://www.conab.gov.br/info-agro/safras/soja (accessed 26 may 2021).

Dekker, R.F.H., Barbosa, A.M., Giese, E.C., Godoy, S.D.S, Covizzi, L.G., 2007. Influence of nutrients on enhancing laccase production by Botryosphaeria rhodina MAMB-05. Int. J. Food Microbiol. 10, 177-186. http://dx.doi.org/10.2436/20.1501.01.25

Eira, A.F., 2004. Edible Fungi, in: Espósito, E., Azevedo, J.L. (Eds.), Fungi an introduction to biology, biochemistry and biotechnology. Educs, Rio Grande do Sul, pp. 379-448.

Eira, A.F., Minhoni, M.T.A., 1997. Practical theoretical manual of the cultivation of edible mushrooms, first ed. FEPAF, São Paulo.

Faria, M.G.I., Avelino, K.V., Valle, J.S., Silva, G.J., Gonçalves Jr, A.C., Dragunski, D.C., Colauto, N.B., Linde, G.A., 2019. Lithium bioaccumulation in Lentinus crinitus mycelial biomass as a potential functional food. Chemosphere 235, 538-542. https://doi.org/10.1016/j.chemosphere.2019.06.218 DOI: https://doi.org/10.1016/j.chemosphere.2019.06.218

Fernandes, A., Barros, L., Martins, A., Herbert, P., Ferreira, I.C., 2015. Nutritional characterisation of Pleurotus ostreatus (Jacq. ex Fr.) P. Kumm. produced using paper scraps as substrate. Food Chem. 169, 396-400. https://doi.org/10.1016/j.foodchem.2014.08.027 DOI: https://doi.org/10.1016/j.foodchem.2014.08.027

Fernandes, L., Lucas, M.S., Maldonado, M.I., Oller, I., Sampaio, A., 2014. Treatment of pulp mill wastewater by Cryptococcus podzolicus and solar photo-Fenton: a case study. Chem. Eng. J. 245, 158–165. https://doi.org/10.1016/j.cej.2014.02.043 DOI: https://doi.org/10.1016/j.cej.2014.02.043

Figueiro, G.G., Graciolli, L.A., 2011. Influence of the chemical composition of the substrate in the cultivation of Pleurotus florida. Ciênc. Agrotec. 35, 924-930. https://doi.org/10.1590/S1413-70542011000500009 DOI: https://doi.org/10.1590/S1413-70542011000500009

Gerrits, J.P.G., 1998. Nutritional and compost, in: Van Griensven, L.J.L.D. (Ed.), The cultivation of mushrooms. Darlington Mushroom Laboratories, England, pp. 525.

He, P., Li, F., Huang, L., Xue, D., Liu, W., Xu, C., 2016. Chemical characterization and antioxidant activity of polysaccharide extract from spent mushroom substrate of Pleurotus eryngii. J. Taiwan Inst. Chem. Eng. 69, 48-53. http://dx.doi.org/10.1016/j.jtice.2016.10.017 DOI: https://doi.org/10.1016/j.jtice.2016.10.017

Jedinak, A., Dudhgaonkar, S., Wu, Q., Simon, J., Silva, D., 2011. Anti-inflammatory activity of edible oyster mushroom is mediated through the inhibition of NF-kB and AP-1 signaling. Nutr. 10, 1-10. https://doi.org/10.1186/1475-2891-10-52 DOI: https://doi.org/10.1186/1475-2891-10-52

Kanagasabapathy, G., Malek, S.N.A., Kuppusamy, U.R., Vikineswary, S. 2011. Chemical Composition and Antioxidant Properties of Extracts of Fresh Fruiting Bodies of Pleurotus sajor-caju (Fr.) Singer. J. Agric. Food Chem. 59, 2618-2626. http://dx.doi.org/10.1021/jf104133g DOI: https://doi.org/10.1021/jf104133g

Kumla, J., Suwannarach, N., Sujarit, K., Penkhrue, W., Kakumyan, P., Jatuwong, K., Vadthanarat, S.; Lumyong, S. 2020. Cultivation of Mushrooms and Their Lignocellulolytic Enzyme Production Through the Utilization of Agro-Industrial Waste. Molecules 25, 1-41. https://doi.org/10.3390/molecules25122811 DOI: https://doi.org/10.3390/molecules25122811

Ito, H., Shimura, K., Itoh, H., Kawade, M., 1997. Antitumor effects of a new polysaccharide-protein complex (ATOM) prepared from Agaricus blazei (Iwade strain 101) “Himematsutake” and its mechanisms in tumor-bearing mice. Anticancer Res. 17, 277–284.

Lisiecka, J., Prasad, R., Jasinska, A., 2021. The Utilisation of Pholiota nameko, Hypsizygus marmoreus, and Hericium erinaceus Spent Mushroom Substrates in Pleurotus ostreatus Cultivation. Horticulturae 7, 1-13. https://doi.org/10.3390/horticulturae7100396 DOI: https://doi.org/10.3390/horticulturae7100396

Ma, G., Yang, W., Zhao, L., Pei, F., Fang, D., Hu, Q., 2018. A Critical Review on the Health Promoting Effects of Mushrooms Nutraceuticals. Food Sci. Hum. Wellness 7, 125-133. https://doi.org/10.1016/j.fshw.2018.05.002 DOI: https://doi.org/10.1016/j.fshw.2018.05.002

Machado, A.R.G. Teixeira, M.F.S., Kirsch, L.S., Campelo, M.C.L., Oliveira, I.M.A., 2016. Nutritional value and proteases of Lentinus citrinus produced by solid state fermentation of lignocellulosic waste from tropical region. Saudi J. Biol. Sci. 23, 621-627. https://doi.org/10.1016/j.sjbs.2015.07.002 DOI: https://doi.org/10.1016/j.sjbs.2015.07.002

Maiti, S., Mallick, S.K., Bhutia, S.K., Behera, B., Mandal, M., Maiti, T.K., 2011. Antitumor effect of culinary-medicinal oyster mushroom, Pleurotus ostreatus (Jacq.: Fr.) P. Kumm., derived protein fraction on tumor-bearing mice models. Int. J. Med. Mushrooms 13, 427-440. https://doi.org/10.1615/intjmedmushr.v13.i5.20 DOI: https://doi.org/10.1615/IntJMedMushr.v13.i5.20

Maity, K.K., Patra, S., Dey, B., Bhunia, S.K., Mandal, S., Das, S., Majumdar, D.K., Maiti, S., Maiti, T.K., Islam, S.S., 2011. A heteropolysaccharide from aqueous extract of an edible mushroom, Pleurotus ostreatus cultivar: structural and biological studies. Carbohydr. Res. 346, 366–372. https://doi.org/10.1016/j.carres.2010.10.026 DOI: https://doi.org/10.1016/j.carres.2010.10.026

Mantovani, T.R.D., Linde, G.A., Colauto, N.B., 2007. Effect of the addition of nitrogen sources to cassava fiber and carbon-to-nitrogen ratios on Agaricus brasiliensis growth. Can. J. Microbiol. 53, 139-143. https://doi.org/10.1139/w06-112 DOI: https://doi.org/10.1139/w06-112

Mattos, L.M., Moretti, C.L., Muniz, L.B., Silva, E.Y.Y., 2009. Analysis protocol for determination of total antioxidant activity in vegetables in the β-carotene/linoleic acid method. https://ainfo.cnptia.embrapa.br/digital/bitstream/CNPH-2010/36126/1/cot-68.pdf (accessed 10 mar 2021).

Mizuno, M., Minato, K., Ito, H., Kawade, M., Terai, H., Tsuchida, H., 1999. Anti-tumor polysaccharide from the mycelium of liquid-cultured Agaricus blazei Murrill. Biochem. Mol. Biol. Int. 47, 704-714. https://doi.org/10.1080/15216549900201773 DOI: https://doi.org/10.1080/15216549900201773

Muszynska, B., Suákowska-ziaja, K., Ekiert, H., 2013. Phenolic acids in selected edible basidiomycota species: Armillaria mellea, Boletus badius, Boletus edulis, Cantharellus cibarius, Lactarius deliciosus and Pleurotus ostreatus. Acta Sci. Pol. Technol. Aliment. 12, 107-116.

Palacios, I., Lozano, M., Moro, C., D’arrigo, M., Rostagno, M.A., Martínez, J.A., García-Lafuente, A., Guillamón, E., Villares, A., 2011. Antioxidant properties of phenolic compounds occurring in edible mushrooms. Food Chem. 128, 674-678. https://doi.org/10.1016/j.foodchem.2011.03.085 DOI: https://doi.org/10.1016/j.foodchem.2011.03.085

Pandey, A., Soccol, C.R., Nigam, P., Soccol, V.T., 2000. Biotechnological potential of agroindustrial residues. I: sugarcane bagasse. Bioresour. Technol. 74, 69-80. https://doi.org/10.1016/S0960-8524(99)00142-X DOI: https://doi.org/10.1016/S0960-8524(99)00142-X

Pegler, D.N., 1997. Preliminary Agaric Flora of East Africa, first ed. Kew Bulletin Additional Series, United States.

Picornell, M.R., Pardo, A., De Juan, J.A., 2015. Reuse of degraded Pleurotus ostreatus substrate through supplementation with wheat bran and Calprozime® quantitative parameters. Agron. colomb. 33, 261-270. https://doi.org/10.15446/agron.colomb.v33n2.49760 DOI: https://doi.org/10.15446/agron.colomb.v33n2.49760

Rampinelli, J.R., Silveira, M.L.L., Gern, R.M.M., Furlan, S.A., Ninow, J.L., Wisbeck, E., 2010. Nutritional value of Pleurotus djamor cultivated on banana straw. Alim. Nutr. 21, 197-202.

Reis, F.S., Martins, A., Barros, L., Ferreira, I.C.F.R., 2012. Antioxidant properties and phenolic profile of the most widely appreciated cultivated mushrooms: A comparative study between in vivo and in vitro samples. Food Chem. Toxicol. 50, 1201-1207. https://doi.org/10.1016/j.fct.2012.02.013 DOI: https://doi.org/10.1016/j.fct.2012.02.013

Rieger, C., Oliveira, V., Lovatto, P.A., Araújo, J.S., Peixoto, E.C.T.M., Silva, M.A., 2008. Chemical characteristics and energy values of soybean meal from western and southwestern Paraná. Cienc. Rural 38, 266-269. http://dx.doi.org/10.1590/S0103-84782008000100046 DOI: https://doi.org/10.1590/S0103-84782008000100046

Rinker, D.L., 2002. Handling and using "spent" mushroom substrate around the world, in: Proceedings of the 4th International Conference of Mushroom Biology and Mushroom Products. World Wide Production of Mushrooms, Cuernavaca, pp. 43-60.

Royse, D.J., Baars, J., Tan, Q., 2017. Current Overview of Mushroom Production in the World, in: Zied, D.C., Pardo-Gimenez, A. (Eds.), Edible and Medicinal Mushrooms. Wiley-Blackwell, England, pp. 5-13. http://dx.doi.org/10.1002/9781119149446.ch2 DOI: https://doi.org/10.1002/9781119149446.ch2

Rufino, M.S.M., Alves, R.E., Brito, E.S., Morais, S.M., Sampaio, C.G., Perez-Jimenez, J., Saura-Calixto, F.D., 2006. Scientific methodology: determination of total antioxidant activity in fruits by the iron reduction method (FRAP). https://ainfo.cnptia.embrapa.br/digital/bitstream/CNPAT-2010/11964/1/cot-125.pdf (accessed 10 mar 2021).

Sanchez-Moreno, C., Larrauri, J.A., Saura-Calixto, F., 1998. A procedure to measure the antiradical efficiency of polyphenols. J. Sci. Food Agric. 76, 270-276. https://doi.org/10.1002/(SICI)1097-0010(199802)76:2<270::AID-JSFA945>3.0.CO;2-9 DOI: https://doi.org/10.1002/(SICI)1097-0010(199802)76:2<270::AID-JSFA945>3.0.CO;2-9

Salata, A., Lemieszek, M., Parzymies, M., 2018. The nutritional and health properties of an oyster mushroom (Pleurotus ostreatus (Jacq. Fr) P. Kumm.). Acta Sci. Pol. Hortorum Cultus 17, 185-197. https://doi.org/10.24326/asphc.2018.2.16 DOI: https://doi.org/10.24326/asphc.2018.2.16

Sardar, H., Ali, M.A., Anjum, M.A., Nawaz, F., Hussain, S., Naz, S., Karimi, S.M., 2017. Agro-industrial residues influence mineral elements accumulation and nutritional composition of king oyster mushroom (Pleurotus eryngii). Sci. Hortic. 225, 327-334. http://dx.doi.org/10.1016/j.scienta.2017.07.010 DOI: https://doi.org/10.1016/j.scienta.2017.07.010

Silva Neto, C. M., Pinto, D.S., Santos, L.A.C., Calaça, F.J.S., 2020. Bromatological aspects of Lentinus crinitus mushroom (Basidiomycota: Polyporaceae) in agroforestry in the Cerrado. Food Sci. Technol. 40, 659-664. https://doi.org/10.1590/fst.14719 DOI: https://doi.org/10.1590/fst.14719

Siqueira, O.A.P.A., Zanon, A.R., Martins, O.G., Andrade, M.C.N., 2016. New substrates for the cultivation of Pleurotus ostreatus using exhausted compost. Afr. J. Agric. Res. 11, 2295-2301. http://dx.doi.org/10.5897/AJAR2016.11009 DOI: https://doi.org/10.5897/AJAR2016.11009

Stojkovic, D., Reis, F.S., Glamoclija, J., Ciric, A., Barros, L., Griensven, L.J.L.D.V., Ferreira, I.C.F.R., Sokovic, M., 2014. Cultivated strains of Agaricus bisporus and A. brasiliensis: chemical characterization and evaluation of antioxidant and antimicrobial properties for the final healthy product – natural preservatives in yoghurt. Food Funct. 5, 1602-1612. https://doi.org/10.1039/c4fo00054d DOI: https://doi.org/10.1039/c4fo00054d

Tanaka, H.S., Bertéli, M.B.D., Cordeiro, F.A., Lopes, A.D., Valle, J.S., Linde, G.A., Colauto, N.B., 2019. Semisolid culture medium improves mycelial recovery of Agaricus subrufescens cryopreserved in cereal grains. Braz. J. Microbiol. 50, 527-532. http://dx.doi.org/10.1007/s42770-019-00063-9 DOI: https://doi.org/10.1007/s42770-019-00063-9

Tavares, M.F., Avelino, K.V., Araújo, N.L., Marim, R.A., Linde, G.A., Colauto, N.B., Valle, J.S., 2020. Decolorization of azo and anthraquinone dyes by crude laccase produced by Lentinus crinitus in solid state cultivation. Braz. J. Microbiol. 51, 99-106. https://doi.org/10.1007/s42770-019-00189-w DOI: https://doi.org/10.1007/s42770-019-00189-w

Vargas-Isla, R., Ishikawa, K.N., Py-Daniel, V., 2013. Ethnomycologic contributions of the Amazonian indigenous people. Biota Amazôn. 3, 58-65. http://dx.doi.org/10.18561/2179-5746/biotaamazonia.v3n1p58-65 DOI: https://doi.org/10.18561/2179-5746/biotaamazonia.v3n1p58-65

Wang, S., Xu, F., LI, Z., Zhao, S., Song, S., Rong, C., Geng, X., Liu, Y., 2015. The spent mushroom substrates of Hypsizigus marmoreus can be an effective component for growing the oyster mushroom Pleurotus ostreatus. Sci. Hortic. 186, 217–222. http://dx.doi.org/10.1016%2Fj.scienta.2015.02.028 DOI: https://doi.org/10.1016/j.scienta.2015.02.028

Yilmaz, A., Yildiz, S., Kiliç, C., Can, Z., 2017. Total Phenolics, Flavonoids, Tannin Contents and Antioxidant Properties of Pleurotus ostreatus Cultivated on Different Wastes and Sawdust. Int. J. Sec. Metabolite 4, p. 1-9. http://dx.doi.org/10.21448/ijsm.252052 DOI: https://doi.org/10.21448/ijsm.252052

Zenebon, O., Pascuet, N.S., Tiglea, P., 2008. Physicochemical methods for food analysis, fourth ed. Instituto Adolfo Lutz, São Paulo.

Zied, D.C., Sanchez, J.E., Noble, R., Pardo-Gimenez, A., 2020. Use of Spent Mushroom Substrate in New Mushroom Crops to Promote the Transition towards a Circular Economy. Agronomy, 10, 1239. http://doi.org/10.3390/agronomy1009123 DOI: https://doi.org/10.3390/agronomy10091239

Downloads

Published

2026-05-11

How to Cite

Use of spent mushroom substrate (SMS) in new production cycles and evaluation of the antioxidant activity of Lentinus crinitus and Pleurotus spp. (2026). REMUNOM, 13(09), 1-27. https://doi.org/10.66104/m58yet98