Skip to main content
SpringerLink
Log in

Spent mushroom substrate of Pleurotus pulmonarius: a source of easily hydrolyzable lignocellulose

  • Published:
Folia Microbiologica Aims and scope Submit manuscript

Abstract

Pleurotus pulmonarius was cultivated on a corncob-based substrate for producing of mushrooms and for assessing the transformation of the lignocellulosics during the development of fungal biomass. Associated events, such as the release of relevant enzymes and the H2O2 generation, were also monitored. The peaks of laccase and catalase activities occurred at the 5th day and that of Mn peroxidase at the 30th day, simultaneously with a high activity of superoxide dismutase. Increase in the endocellulase and xylanase activities was observed after 10 days, with maximal activities achieved during the 20–30-day period. Maximal values of H2O2 were found after 10 days of cultivation. Electron microscopy and Fourier transform infrared (FTIR) spectroscopy showed strong alterations in the lignocellulosic fibers. The uncultivated and the cultivated substrates at different times were hydrolyzed with commercial cellulase and β-glucosidase. The highest values of reducing sugars (110.5 ± 5.6 μmol/mL), being 65 % glucose, were obtained using the 20-day cultivated substrate. After the fruiting stage (first flush), enzymatic hydrolysis of the spent mushroom substrate (SMS) yielded 53.0 ± 2.8 and 77.5 ± 4.0 μmol/mL of glucose and total reducing sugars, respectively. Although the release of reducing sugars of the P. pulmonarius SMS was lower than that obtained after 20 days of cultivation, it was still 50 % higher than that obtained using the uncultured substrate. This observation, combined with the fact that SMS constitutes a residue generated as a by-product of the depletion of an agro-industrial residue, allows to conclude that this material offers an interesting economic perspective for the obtainment of cellulosic ethanol.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • Alananbeh KM, Bougellah NA, Al Kaff NS (2014) Cultivation of oyster mushroom Pleurotus ostreatus on date-palm leaves mixed with other agro-wastes in Saudi Arabia. Saudi J Biol Sci 21:616–625

    Article  PubMed  PubMed Central  Google Scholar 

  • Bazanella GCS, de Souza DF, Castoldi R, Oliveira RF, Bracht A, Peralta RM (2013) Production of laccase and manganese peroxidase by Pleurotus pulmonarius in solid-state cultures and application in dye decolorization. Folia Microbiol 58:641–647

    Article  CAS  Google Scholar 

  • Casas A, Palomar J, Alonso MV, Oliet M, Omar S, Rodriguez F (2012) Comparison of lignin and cellulose solubilities in ionic liquids by COSMO-RS analysis and experimental validation. Ind Crop Prod 37:155–163

    Article  CAS  Google Scholar 

  • Castoldi R, Bracht A, de Morais GR, Baesso ML, Correa RCG, Peralta RA, Moreira RFPM, Polizeli MLTM, de Souza CGM, Peralta RM (2014) Biological pretreatment of Eucalyptus grandis sawdust with white-rot fungi: study of degradation patterns and saccharification kinetics. Chem Eng J 258:240–246

    Article  CAS  Google Scholar 

  • Chen GQ, Zeng GM, Tu X, Huang GH, Chen YN (2005) A novel biosorbent: characterization of the spent mushroom compost and its application for removal of heavy metals. J Environ Sci 17:756–760

    CAS  Google Scholar 

  • Chen Y, Dai J, Zhou X, Liu Y, Zhang W, Peng G (2014) Raman spectroscopy analysis of the biochemical characteristics of molecules associated with the malignant transformation of gastric mucosa. PLoS One 9:e93906

    Article  PubMed  PubMed Central  Google Scholar 

  • Cherian BM, Pothan LA, Nguyen-Chung T, Mennig G, Kottaisamy M, Tomas S (2008) A novel method for the synthesis of celulose nanofibril whiskers from banana fibers and characterization. J Agric Food Chem 56:5617–5627

    Article  CAS  PubMed  Google Scholar 

  • Chiu S-W, Gao T, Chan CS-S, Ho CK-M (2009) Removal of spilled petroleum in industrial soils by spent compost of mushroom Pleurotus pulmonarius. Chemosphere 75:837–842

    Article  CAS  PubMed  Google Scholar 

  • Elisashvili V, Chichua D, Kachlisvili E, Tsiklauri N, Khardziani T (2003) Lignocellulolytic enzyme activity during growth and fruiting of the edible and medicinal mushroom Pleurotus ostreatus (Jacq.:Fr.) Kumm. Int J Med Mushrooms 5:193–198

    Article  CAS  Google Scholar 

  • Fazaeli H, Talebian-Masoodi AR (2006) Spent wheat straw compost of Agaricus bisporus mushroom as ruminant feed. Asian Australas J Anim Sci 19:845–851

    Article  CAS  Google Scholar 

  • Finney KN, Ryu C, Sharifi VN, Swithenbank J (2009) The reuse of spent mushroom compost and coal tailings for energy recovery: comparison of thermal treatment technologies. Bioresour Technol 100:310–315

    Article  CAS  PubMed  Google Scholar 

  • Ghose TK (1987) Measurement of cellulase activity. Pure Appl Chem 59:257–268

    CAS  Google Scholar 

  • Ginterová A, Lazarová A (1987) Degradation dynamics of lignocellulose materials by wood-rotting Pleurotus fungi. Folia Microbiol 32:434–437

    Article  Google Scholar 

  • Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315:804–807

    Article  CAS  PubMed  Google Scholar 

  • Hou H, Zhou J, Wang J, Du C, Yan B (2004) Enhancement of laccase production by Pleurotus ostreatus and its use for the decolorization of anthraquinone dye. Proc Biochem 30:1415–1419

    Article  Google Scholar 

  • Ibarra D, del Rio JC, Gutiérrez A, Rodríguez IM, Romero J, Martinez MJ, Martinez AT (2004) Isolation of high-purity residual lignins from eucalypt paper pulps by cellulase and proteinase treatments followed by solvent extraction. Enzym Microb Technol 35:173–181

    Article  CAS  Google Scholar 

  • Juárez RAC, Dorry LLG, Bello-Mendoza R, Sánchez JE (2011) Use of spent substrate after Pleurotus pulmonarius cultivation for the treatment of chlorothalonil containing wastewater. J Environ Manag 92:948–952

    Article  Google Scholar 

  • Kapu NUS, Manning M, Hurley TB, Voigt J, Cosgrove DJ, Romaine CP (2012) Surfactant-assisted pretreatment and enzymatic hydrolysis of spent mushroom compost for the production of sugars. Bioresour Technol 114:399–405

    Article  CAS  PubMed  Google Scholar 

  • Kesheri M, Kanchan S, Richa SRP (2014) Isolation and in silico analysis of Fe-superoxide dismutase in the cyanobacterium Nostoc commune. Gene 553:117–125

    Article  CAS  PubMed  Google Scholar 

  • Ko HG, Park SH, Kim SH, Park HG, Park WM (2005) Detection and recovery of hydrolytic enzymes from spent compost of four mushroom species. Folia Microbiol 50:103–106

    Article  CAS  Google Scholar 

  • Kurt S, Buyukalaca S (2010) Yield performances and changes in enzyme activities of Pleurotus spp (P. ostreatus and P. sajor-caju) cultivated on different agricultural wastes. Bioresour Technol 101:3164–3169

    Article  CAS  PubMed  Google Scholar 

  • Lau KL, Tsang YY, Chiu SW (2003) Use of spent mushroom compost to bioremediate PAH-contaminated samples. Chemosphere 52:1539–1546

    Article  CAS  PubMed  Google Scholar 

  • Lenartovicz V, Souza CGM, Moreira FG, Peralta RM (2003) Temperature and carbon source affect the production and secretion of a thermostable β-xylosidase by Aspergillus fumigatus. Proc Biochem 38:1775–1780

    Article  CAS  Google Scholar 

  • Lin Y, Ge X, Li Y (2014) Solid-state anaerobic co-digestion of spent mushroom substrate with yard trimmings and wheat straw for biogas production. Bioresour Technol 169:468–474

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Wang Q, Sun X, Wang X, Su W, Song N (2014) A study on recycling of spent mushroom substrate to prepare chairs and activated carbon. Bioresources 9:3939–3954

    Google Scholar 

  • Marklund S, Marklun G (1974) Involvement of superoxide anion radical in autoxidation of pyrogallol and a convenient assay for superoxide-dismutase. Eur J Biochem 47:469–474

    Article  CAS  PubMed  Google Scholar 

  • Mayolo-Deloisa K, Trejo-Hernández MDR, Rito-Palomares M (2009) Recovery of laccase from the residual compost of Agaricus bisporus in aqueous two-phase systems. Proc Biochem 44:435–439

    Article  CAS  Google Scholar 

  • Miller GL (1959) Dinitrosalicylic acid reagent for determination of reducing sugars. Anal Chem 31:426–428

    Article  CAS  Google Scholar 

  • Milton RD, Minteera SD (2014) Investigating the reversible inhibition model of laccase by hydrogen peroxide for bioelectrocatalytic applications. J Electrochem Soc 161:H3011–H3014

    Article  Google Scholar 

  • Mosier N, Wyman C, Dale B, Elander R, Lee YY, Holtzapple M, Ladisch M (2005) Features of promissing technologies for pretreatment of lignocellulosic biomass. Bioresour Technol 96:673–686

    Article  CAS  PubMed  Google Scholar 

  • Oliveira MA, Donega MA, Peralta RM, Souza CGM (2007) Production of spawn for edible mushroom Pleurotus pulmonarius (Fr.) Quélet - CCB19 using agricultural wastes. Cienc Tecnol Aliment 27:84–87

    Article  Google Scholar 

  • Pandey KK, Pitman AJ (2003) FTIR studies of the changes in wood chemistry following decay by brown-rot and white-rot fungi. Int Biodeterior Biodegrad 52:151–160

    Article  CAS  Google Scholar 

  • Phan C-W, Sabaratnam V (2012) Potential uses of spent mushroom substrate and its associated lignocellulosic enzymes. Appl Microbiol Biotechnol 96:863–873

    Article  CAS  PubMed  Google Scholar 

  • Rajarathnan S, Wankhede DB, Bano Z (1987) Degradation of rice straw by Pleurotus flabellatus. J Chem Tech Biotechnol 37:203–214

  • Ribas LCC, de Mendonça MM, Camelini CM, Soares CHL (2009) Use of spent mushroom substrates from Agaricus subrufescens (syn. A. blazei, A. brasiliensis) and Lentinula edodes productions in the enrichment of a soil-based potting media for lettuce (Lactuca sativa) cultivation: growth promotion and soil bioremediation. Bioresour Technol 100:4750–4757

    Article  CAS  PubMed  Google Scholar 

  • Rinker DL (2002) Handling and using “spent” mushroom substrate around the world. In: Sanchez JE, et al (eds) Proceedings of the Fourth International conference on mushroom biology and mushroom products, February 20–23, Cuernavaca, Mexico, pp 43–60

  • Scotti CT, Vergoignan C, Feron G, Durand A (2001) Glucosamine measurement as indirect method for biomass of Cunninghamella elegans grown in solid state cultivation conditions. Biochem Eng J 7:1–5

    Article  CAS  PubMed  Google Scholar 

  • Silva SO, Costa SMG, Clemente E (2002) Chemical composition of Pleurotus pulmonarius (Fr.) Quél., substrates and residue, after cultivation. Braz Arch Biol Technol 45:531–535

    Article  CAS  Google Scholar 

  • Simmons BA, Loque D, Ralph J (2010) Advances in modifying lignin for enhanced biofuel production. Curr Opin Plant Biol 13:312–319

    Article  Google Scholar 

  • Sindhu R, Binod P, Pandey A (2016) Biological pretreatment of lignocellulosic biomass: an overview. Bioresour Technol 199:76–82

    Article  CAS  PubMed  Google Scholar 

  • Singh AD, Abdullah N, Vikineswary S (2003) Optimization of extraction of bulk enzymes from spent mushroom compost. J Chem Technol Biotechnol 78:743–752

    Article  CAS  Google Scholar 

  • Singh AD, Sabaratnam V, Abdullah N, Annuar MSM, Ramachandran KB (2010) Decolourisation of chemically different dyes by enzymes from spent compost of Pleurotus sajor-caju and their kinetics. Afr J Biotechnol 9:41–54

    CAS  Google Scholar 

  • Singh AD, Vikineswary S, Abdullah N, Sekaran M (2011) Enzymes from spent mushroom substrate of Pleurotus sajor-caju for the decolourisation and detoxification of textile dyes. World J Microbiol Biotechnol 27:535–545

    Article  CAS  Google Scholar 

  • Siqueira G, Bras J, Dufresne A (2010) Luffa cylindrica as a lignocellulosic source of fiber, microfibrillated cellulose, and cellulose nanocrystals. BioResources 5:727–740

    CAS  Google Scholar 

  • Siqueira IR, Fochesatto C, Torres ILS, Dalmaz C, Netto CA (2005) Aging affects oxidative state in hippocampus, hypothalamus and adrenal glands of Wistar rats. Life Sci 78:271–278

    Article  Google Scholar 

  • Sun F-H, Li J, Yuan Y-X, Yan Z-Y, Liu X-F (2011) Effect of biological pretreatment with Trametes hirsuta yj9 on enzymatic hydrolysis of corn stover. Int Biodeterior Biodegrad 65:931–938

    Article  CAS  Google Scholar 

  • Sun Y, Cheng J (2002) Hydrolysis of lignocellulosic materials for ethanol production: a review. Bioresour Technol 83:1–11

    Article  CAS  PubMed  Google Scholar 

  • Toptas A, Demierege S, Ayan EM, Yanik J (2014) Spent mushroom compost as biosorbent for dye biosorption. Clean-Soil Air Water 42:1721–1728

    Article  CAS  Google Scholar 

  • Van Kuijk SJA, Sonnenberg ASM, Baars JJP, Hendriks WH, Cone JW (2015) Fungal treated lignocellulosic biomass as ruminant feed ingredient: a review. Biotechnol Rev 33:191–202

    Google Scholar 

  • Vázquez-Fernández MÁ, Bermejo MR, Fernández-García MI, González-Riopedre G, Rodríguez-Doutón MJ, Maneiro M (2011) Influence of the geometry around the manganese ion on the peroxidase and catalase activities of Mn(III)–Schiff base complexes. J Inorg Biochem 105:1538–1547

    Article  PubMed  Google Scholar 

  • Wariishi H, Valli K, Gold MH (1992) Manganese (II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium. J Biol Chem 267:23688–23695

    CAS  PubMed  Google Scholar 

  • Williams BC, McMullan JT, McCahey S (2001) An initial assessment of spent mushroom compost as a potential energy feedstock. Bioresour Technol 79:227–230

    Article  CAS  PubMed  Google Scholar 

  • Wu S, Lan Y, Wu Z, Peng Y, Chen S, Huang Z, Gelbic I, Guan X, Zhang L, Zou S (2013) Pretreatment of spent mushroom substrate for enhancing the conversion of fermentable sugar. BioresourTechnol 148:596–600

    Article  CAS  Google Scholar 

  • Yu H, Zhang X, Song L, Ke J, Xu C, Du W, Zhang J (2010) Evaluation of white-rot fungi-assisted alkaline/oxidative pretreatment of corn straw undergoing enzymatic hydrolysis by cellulase. J Biosci Bioeng 110:660–664

    Article  CAS  PubMed  Google Scholar 

  • Zhang R-H, Duan Z-Q, Li Z-G (2012) Use of spent mushroom substrate as growing Media for tomato and cucumber seedlings. Pedosphere 22:333–342

    Article  CAS  Google Scholar 

  • Zhang X, Yu H, Huang H, Liu Y (2007) Evaluation of biological pretreatment with white rot fungi for the enzymatic hydrolysis of bamboo culms. Int Biodeterior Biodegrad 60:159–164

    Article  CAS  Google Scholar 

  • Zilly A, Bazanella GCS, Helm CV, Araújo CAV, Souza CGM, Bracht A, Peralta RM (2012) Solid-state bioconversion of passion fruit waste by white-rot fungi for production of oxidative and hydrolytic enzymes. Food Bioproc Technol 5:1573–1580

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), grant 477825/2012-5 for funding this study. Authors R.C.G. Correa and R. Castoldi thank CNPq and Coordenação de Aperfeiçoamento do Pessoal do Ensino Superior (CAPES) for the financial support provided for their post-graduate studies in Universidade Estadual de Maringá. A. Bracht, R.A. Peralta, and R.M. Peralta are research grant recipients of CNPq. The authors thank M.A.F. Costa and A. Chaves by technical assistance.

Author information

Authors and Affiliations

  1. Postgraduate Program of Food Science, State University of Maringá, 87020-900, Maringá, PR, Brazil

    Rúbia Carvalho Gomes Corrêa, Camila Gabriel Kato, Anacharis Babeto de Sá-Nakanishi, Adelar Bracht & Rosane Marina Peralta

  2. Department of Biochemistry, State University of Maringá, 87020-900, Maringá, PR, Brazil

    Bruna Polacchini da Silva, Rafael Castoldi, Anacharis Babeto de Sá-Nakanishi, Cristina G. M. de Souza, Adelar Bracht & Rosane Marina Peralta

  3. Department of Chemistry, Federal University of Santa Catarina, Florianópolis, Brazil

    Rosely Aparecida Peralta

Authors
  1. Rúbia Carvalho Gomes Corrêa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bruna Polacchini da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rafael Castoldi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Camila Gabriel Kato
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anacharis Babeto de Sá-Nakanishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rosely Aparecida Peralta
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cristina G. M. de Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Adelar Bracht
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rosane Marina Peralta
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rosane Marina Peralta.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Corrêa, R.C.G., da Silva, B.P., Castoldi, R. et al. Spent mushroom substrate of Pleurotus pulmonarius: a source of easily hydrolyzable lignocellulose. Folia Microbiol 61, 439–448 (2016). https://doi.org/10.1007/s12223-016-0457-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12223-016-0457-8

Keywords

Search

Navigation