Use of spent mushroom substrate (SMS) in new production cycles and evaluation of the antioxidant activity of Lentinus crinitus and Pleurotus spp.
DOI:
https://doi.org/10.66104/m58yet98Keywords:
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
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
Issue
Section
License
Copyright (c) 2026 Olavo Bilac Quaresma de Oliveira Filho , Miria Benetati Delgado Bertéli, Nelson Barros Colauto, Giani Andrea Linde Colauto, Perseu da Silva Aparicio, William Kalhy Silva Xavier, Carlos Henrique Medeiros de Abreu, Juliana Silveira do Valle

This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish in this journal agree to the following terms:
Authors retain copyright and grant the journal the right of first publication, with the work simultaneously licensed under the Creative Commons Attribution License, which permits the sharing of the work with proper acknowledgment of authorship and initial publication in this journal;
Authors are authorized to enter into separate, additional agreements for the non-exclusive distribution of the version of the work published in this journal (e.g., posting in an institutional repository or publishing it as a book chapter), provided that authorship and initial publication in this journal are properly acknowledged, and that the work is adapted to the template of the respective repository;
Authors are permitted and encouraged to post and distribute their work online (e.g., in institutional repositories or on their personal websites) at any point before or during the editorial process, as this may lead to productive exchanges and increase the impact and citation of the published work (see The Effect of Open Access);
Authors are responsible for correctly providing their personal information, including name, keywords, abstracts, and other relevant data, thereby defining how they wish to be cited. The journal’s editorial board is not responsible for any errors or inconsistencies in these records.
PRIVACY POLICY
The names and email addresses provided to this journal will be used exclusively for the purposes of this publication and will not be made available for any other purpose or to third parties.
Note: All content of the work is the sole responsibility of the author and the advisor.
