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Cellulase production by white-rot basidiomycetous fungi: solid-state versus submerged cultivation

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Abstract

White-rot basidiomycetous (WRB) fungi are a group of wood-decaying fungi that are known to be endowed with the ability to secrete enzymes that can catalyze decomposition of a range of plant cell wall polysaccharides, including cellulose and lignin. Expression of these enzymes is induced by the substrate and the enzyme yields obtained depend on the growth of the fungi and thus the mode of cultivation. In order to exploit WRB fungi for local enzyme production for converting lignocellulosic materials in biorefinery processes, the fungi can principally be cultivated in either solid-state (SSC) or submerged cultivation (SmC) systems. In this review, we quantitatively assess the data available in the literature on cellulase production yields by WRB fungi cultivated by SSC or SmC. The review also assesses cellulolytic enzyme production rates and enzyme recovery when WRB fungi are cultivated on different biomass residues in SSC or SmC systems. Although some variation in cellulase production yields have been reported for certain substrates, the analysis convincingly shows that SmC is generally more efficient than SSC for obtaining high cellulase production yields and high cellulase production rates on the substrate used. However, the cultivation method also affects the enzyme activity profile obtained, and the resulting enzyme titers and significant dilution of the enzymes usually occurs in SmC. The review also highlights some future approaches, including sequential cultivations and co-cultivation of WRB fungi for improved enzyme expression, as well as on-site approaches for production of enzyme blends for industrial biomass conversion. The quantitative comparisons made have implications for selection of the most appropriate cultivation method for WRB fungi for attaining maximal cellulase production.

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References

  • Amigun B, Sigamoney R, von Blottnitz H (2008) Commercialisation of biofuel industry in Africa: a review. Renew Sust Energ Rev 12:690–711. https://doi.org/10.1016/j.rser.2006.10.019

    Article  Google Scholar 

  • An Q, Wu X, Han M, Cui B, He S, Dai Y, Si J (2016) Sequential solid-state and submerged cultivation of the white rot fungus Pleurotus ostreatus on biomass and the activity of lignocellulolytic enzymes. Bioresources 11:8791–8805. https://doi.org/10.15376/biores.11.4.8791-8805

    Article  CAS  Google Scholar 

  • Anwar Z, Gulfraz M, Irshad M (2014) Agro-industrial lignocellulosic biomass a key to unlock the future bio-energy: a brief review. J Radiat Res Appl Sci 7:163–173. https://doi.org/10.1016/j.jrras.2014.02.003

    Article  CAS  Google Scholar 

  • Arora S, Rani R, Ghosh S (2018) Bioreactors in solid state fermentation technology: design, applications and engineering aspects. J Biotechnol 269:16–34. https://doi.org/10.1016/j.jbiotec.2018.01.010

    Article  PubMed  CAS  Google Scholar 

  • Baldrian P, Valaskova V (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 32:501–521. https://doi.org/10.1111/j.1574-6976.2008.00106.x

    Article  PubMed  CAS  Google Scholar 

  • Bentil JA, Dzogbefia VP, Alemawor F (2015) Enhancement of the nutritive value of cocoa (Theobroma cacao) bean shells for use as feed for animals through a two-stage solid state fermentation with Pleurotus ostreatus and Aspergillus niger. Int J Appl Microbiol Biotechnol Res 3:20–30

    Google Scholar 

  • Binder M, Justo A, Riley R, Salamov A, Lopez-Giraldez F, Sjokvist E, Copeland A, Foster B, Sun H, Larsson E, Larsson K-H, Townsend J, Grigoriev IV, Hibbett DS (2013) Phylogenetic and phylogenomic overview of the Polyporales. Mycologia 105:1350–1373. https://doi.org/10.3852/13-003

    Article  PubMed  CAS  Google Scholar 

  • Busk PK, Lange M, Pilgaard B, Lange L (2014) Several genes encoding enzymes with the same activity are necessary for aerobic fungal degradation of cellulose in nature. PLoS One 9:e114138. https://doi.org/10.1371/journal.pone.0114138

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cai Y, Gong Y, Liu W, Hu Y, Chen L, Yan L, Zhou Y, Bian Y (2017) Comparative secretomic analysis of lignocellulose degradation by Lentinula edodes grown on microcrystalline cellulose, lignosulfonate and glucose. J Proteome 163:92–101. https://doi.org/10.1016/j.jprot.2017.04.023

    Article  CAS  Google Scholar 

  • Carabajal M, Levin L, Albertó E, Lechner B (2012) Effect of co-cultivation of two Pleurotus species on lignocellulolytic enzyme production and mushroom fructification. Int Biodeterior Biodegrad 66:71–76. https://doi.org/10.1016/j.ibiod.2011.11.002

    Article  CAS  Google Scholar 

  • Chen H, He Q (2013) A novel structured bioreactor for solid-state fermentation. Bioprocess Biosyst Eng 36:223–230. https://doi.org/10.1007/s00449-012-0778-1

    Article  PubMed  CAS  Google Scholar 

  • Chen S, Xu J, Liu C, Zhu Y, Nelson DR, Zhou S, Li C, Wang L, Guo X, Sun Y, Luo H, Li Y, Song J, Henrissat B, Levasseur A, Qian J, Li J, Luo X, Shi L, He L, Xiang L, Xu X, Niu Y, Li Q, Han MV, Yan H, Zhang J, Chen H, Lv A, Wang Z, Liu M, Schwartz DC, Sun C (2012) Genome sequence of the model medicinal mushroom Ganoderma lucidum. Nat Commun 3:913. https://doi.org/10.1038/ncomms1923

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cianchetta S, Galletti S, Burzi PL, Cerato C (2012) Hydrolytic potential of Trichoderma sp. strains evaluated by microplate-based screening followed by switchgrass saccharification. Enzym Microb Technol 50:304–310. https://doi.org/10.1016/j.enzmictec.2012.02.005

    Article  CAS  Google Scholar 

  • Coutinho PM, Andersen MR, Kolenova K, VanKuyk PA, Benoit I, Gruben BS, Trejo-Aguilar B, Visser H, van Solingen P, Pakula T, Seiboth B, Battaglia E, Aguilar-Osorio G, de Jong JF, Ohm RA, Aguilar M, Henrissat B, Nielsen J, Stålbrand H, de Vries RP (2009) Post-genomic insights into the plant polysaccharide degradation potential of Aspergillus nidulans and comparison to Aspergillus niger and Aspergillus oryzae. Fungal Genet Biol 46(Suppl 1):S161–S169. https://doi.org/10.1016/j.fgb.2008.07.020

    Article  PubMed  CAS  Google Scholar 

  • Cragg SM, Beckham GT, Bruce NC, Bugg TDH, Distel DL, Dupree P, Etxabe AG, Goodell BS, Jellison J, McGeehan JE, McQueen-Mason SJ, Schnorr K, Walton PH, Watts JEM, Zimmer M (2015) Lignocellulose degradation mechanisms across the tree of life. Curr Opin Chem Biol 29:108–119. https://doi.org/10.1016/j.cbpa.2015.10.018

    Article  PubMed  CAS  Google Scholar 

  • Cunha FM, Esperanca MN, Zangirolami TC, Badino AC, Farinas CS (2012) Sequential solid-state and submerged cultivation of Aspergillus niger on sugarcane bagasse for the production of cellulase. Bioresour Technol 112:270–274. https://doi.org/10.1016/j.biortech.2012.02.082

    Article  PubMed  CAS  Google Scholar 

  • Cunha FM, Vasconcellos VM, Florencia C, Badino AC, Farinas CS (2017) On-site production of enzymatic cocktails using a non-conventional fermentation method with agro-industrial residues as renewable feedstocks. Waste Biomass Valor 8:517–526. https://doi.org/10.1007/s12649-016-9609-y

    Article  CAS  Google Scholar 

  • da Silva Delabona P, Farinas CS, da Silva MR, Azzoni SF, da Cruz Pradella JG (2012) Use of a new Trichoderma harzianum strain isolated from the Amazon rainforest with pretreated sugar cane bagasse for on-site cellulase production. Bioresour Technol 107:517–521. https://doi.org/10.1016/j.biortech.2011.12.048

    Article  CAS  Google Scholar 

  • Dong YC, Wang W, Hu ZC, Fu ML, Chen QH (2012) The synergistic effect on production of lignin-modifying enzymes through submerged co-cultivation of Phlebia radiata, Dichomitus squalens and Ceriporiopsis subvermispora using agricultural residues. Bioprocess Biosyst Eng 35:751–760. https://doi.org/10.1007/s00449-011-0655-3

    Article  PubMed  CAS  Google Scholar 

  • Dong YC, Dai YN, Xu TY, Cai J, Chen QH (2014) Biodegradation of chestnut shell and lignin-modifying enzymes production by the white-rot fungi Dichomitus squalens, Phlebia radiata. Bioprocess Biosyst Eng 37:755–764. https://doi.org/10.1007/s00449-013-1045-9

    Article  PubMed  CAS  Google Scholar 

  • Durand A (2003) Bioreactor designs for solid state fermentation. Biochem Eng J 13:113–125. https://doi.org/10.1016/S1369-703X(02)00124-9

    Article  CAS  Google Scholar 

  • Elisashvili V, Kachlishvili E, Penninckx M (2008a) Effect of growth substrate, method of fermentation, and nitrogen source on lignocellulose-degrading enzymes production by white-rot basidiomycetes. J Ind Microbiol Biotechnol 35:1531–1538. https://doi.org/10.1007/s10295-008-0454-2

    Article  PubMed  CAS  Google Scholar 

  • Elisashvili V, Penninckx M, Kachlishvili E, Tsiklauri N, Metreveli E, Kharziani T, Kvesitadze G (2008b) Lentinus edodes and Pleurotus species lignocellulolytic enzymes activity in submerged and solid-state fermentation of lignocellulosic wastes of different composition. Bioresour Technol 99:457–462. https://doi.org/10.1016/j.biortech.2007.01.011

    Article  PubMed  CAS  Google Scholar 

  • Elisashvili V, Kachlishvili E, Tsiklauri N, Metreveli E, Khardziani T, Agathos SN (2009) Lignocellulose-degrading enzyme production by white-rot basidiomycetes isolated from the forests of Georgia. World J Microbiol Biotechnol 25:331–339. https://doi.org/10.1007/s11274-008-9897-x

    Article  CAS  Google Scholar 

  • Fernandez-Fueyo E, Ruiz-Dueñas FJ, Ferreira P, Floudas D, Hibbett DD, Canessa P, Larrondo LF, James TY, Seelenfreund D, Lobos S, Polanco R, Tello M, Honda Y, Watanabe T, Watanabe T, San RJ, Kubicek CP, Schmoll M, Gaskell J, Hammel KE, St. John FJ, Wymelenberg AV, Sabat G, BonDurant SP, Syed K, Yadav JS, Dodda-paneni H, Subramanian V, Lavín JL, Oguiza JA, Gumer P, Pisabarro AG, Ramirez L, Santoyo F, Master E, Coutinho PM, Henrissat B, Lombard V, Magnuson JK, Kües U, Hori C, Igarashi K, Samejima M, Held BW, Barry KW, LaButti KM, Lapidus A, Lindquist EA, Lucas SM, Riley R, Salamov AA, Hoffmeister D, Schwenk D, Hadar Y, Yarden O, de Vries RP, Wiebenga A, Stenlid J, Eastwood D, Grigoriev IV, Berka RM, Blanchette RA, Kersten P, Martinez AT, Vicuna R, Cullen D (2012) Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. Proc Natl Acad Sci 109:5458–5463. https://doi.org/10.1073/pnas.1119912109

    Article  PubMed  PubMed Central  Google Scholar 

  • Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Górecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kües U, Kumar TKA, Kuo A, LaButti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Dueñas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, St. John F, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719. https://doi.org/10.1126/science.1221748

    Article  PubMed  CAS  Google Scholar 

  • Govumoni SP, Gentela J, Koti S, Haragopal V, Venkateshwar S, Rao LV (2015) Extracellular lignocellulolytic enzymes by Phanerochaete chrysosporium (MTCC 787) under solid-state fermentation of agro wastes. Int J Curr Microbiol App Sci 4:700–710

    CAS  Google Scholar 

  • Heidorne FO, Magalhaes PO, Ferraz AL, Milagres AMF (2006) Characterization of hemicellulases and cellulases produced by Ceriporiopsis subvermispora grown on wood under biopulping conditions. Enzym Microb Technol 38:436–442. https://doi.org/10.1016/j.enzmictec.2005.06.015

    Article  CAS  Google Scholar 

  • Ibrahim D, Weloosamy H, Lim S (2015) Effect of agitation speed on the morphology of Aspergillus niger HFD5A-1 hyphae and its pectinase production in submerged fermentation. World J Biol Chem 6:265–271. https://doi.org/10.4331/wjbc.v6.i3.265

    Article  PubMed  PubMed Central  Google Scholar 

  • Isaksen T, Westereng B, Aachmann FL, Agger JW, Kracher D, Kittl R, Ludwig R, Haltrich D, Eijsink VGH, Horn SJ (2014) A C4-oxidizing lytic polysaccharide mono-oxygenase cleaving both cellulose and cello-oligosaccharides. J Biol Chem 289:2632–2642. https://doi.org/10.1074/jbc.M113.530196

    Article  PubMed  CAS  Google Scholar 

  • Kachlishvili E, Penninckx MJ, Tsiklauri N, Elisashvili V (2006) Effect of nitrogen source on lignocellulolytic enzyme production by white-rot basidiomycetes under solid-state cultivation. World J Microbiol Biotechnol 22:391–397. https://doi.org/10.1007/s11274-005-9046-8

    Article  CAS  Google Scholar 

  • Kannaiyan R, Mahinpey N, Kostenko V, Martinuzzi RJ (2015) Nutrient media optimization for simultaneous enhancement of the laccase and peroxidases production by coculture of Dichomitus squalens and Ceriporiopsis subvermispora. Biotechnol Appl Biochem 62:173–185. https://doi.org/10.1002/bab.1263

    Article  PubMed  CAS  Google Scholar 

  • Khalil AI (2002) Production and characterization of cellulolytic and xylanolytic enzymes from the ligninolytic white-rot fungus Phanerochaete chrysosporium grown on sugarcane bagasse. World J Microbiol Biotechnol 18:753–759. https://doi.org/10.1023/A:1020483618186

    Article  CAS  Google Scholar 

  • Khalil MI, Hoque MM, Basunia MA, Alam N, Khan MA (2011) Production of cellulase by Pleurotus ostreatus and Pleurotus sajor-caju in solid state fermentation of lignocellulosic biomass. Turkish J Agric For 35:333–341. https://doi.org/10.3906/tar-1002-684

    Article  CAS  Google Scholar 

  • Kuhad RC, Gupta R, Singh A (2011) Microbial cellulases and their industrial applications. Enzyme Res 2011:280696. https://doi.org/10.4061/2011/280696

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuhar F, Castiglia V, Levin L (2015) Enhancement of laccase production and malachite green decolorization by co-culturing Ganoderma lucidum and Trametes versicolor in solid-state fermentation. Int Biodeter Biodegrad 104:238–243. https://doi.org/10.1016/j.ibiod.2015.06.017

    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. https://doi.org/10.1016/j.biortech.2009.12.011

    Article  PubMed  CAS  Google Scholar 

  • Lechner BE, Papinutti VL (2006) Production of lignocellulosic enzymes during growth and fruiting of the edible fungus Lentinus tigrinus on wheat straw. Process Biochem 41:594–598. https://doi.org/10.1016/j.procbio.2005.08.004

    Article  CAS  Google Scholar 

  • Lenfant N, Hainaut M, Terrapon N, Drula E, Lombard V, Henrissat B (2017) A bioinformatics analysis of 3400 lytic polysaccharide oxidases from family AA9. Carbohydr Res 448:166–174. https://doi.org/10.1016/j.carres.2017.04.012

    Article  PubMed  CAS  Google Scholar 

  • Levin L, Herrmann C, Papinutti VL (2008) Optimization of lignocellulolytic enzyme production by the white-rot fungus Trametes trogii in solid-state fermentation using response surface methodology. Biochem Eng J 39:207–214. https://doi.org/10.1016/j.bej.2007.09.004

    Article  CAS  Google Scholar 

  • Lombard V, Ramulu HG, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495. https://doi.org/10.1093/nar/gkt1178

    Article  PubMed  CAS  Google Scholar 

  • Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577. https://doi.org/10.1128/MMBR.66.3.506

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lynd LR, Sow M, Chimphango AFA, Cortez LAB, Cruz CHB, Elmissiry M, Laser M, Mayaki IA, Moraes MAFD, Nogueira LAH, Wolfaardt GM, Woods J, van Zyl WH (2015) Bioenergy and African transformation. Biotechnol Biofuels 8:18. https://doi.org/10.1186/s13068-014-0188-5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Martínez ÁT, Speranza M, Ruiz-Dueñas FJ, Ferreira P, Camarero S, Guillén F, Martínez MJ, Gutiérrez A, del Río JC (2005) Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol 8:195–204

    PubMed  Google Scholar 

  • Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P, Hammel KE, Vanden Wymelenberg A, Gaskell J, Lindquist E, Sabat G, Bondurant SS, Larrondo LF, Canessa P, Vicuna R, Yadav J, Doddapaneni H, Subramanian V, Pisabarro AG, Lavin JL, Oguiza JA, Master E, Henrissat B, Coutinho PM, Harris P, Magnuson JK, Baker SE, Bruno K, Kenealy W, Hoegger PJ, Kues U, Ramaiya P, Lucas S, Salamov A, Shapiro H, Tu H, Chee CL, Misra M, Xie G, Teter S, Yaver D, James T, Mokrejs M, Pospisek M, Grigoriev IV, Brettin T, Rokhsar D, Berka R, Cullen D (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci U S A 106:1954–1959. https://doi.org/10.1073/pnas.0809575106

    Article  PubMed  PubMed Central  Google Scholar 

  • Maurya DP, Singh D, Pratap D, Maurya JP (2012) Optimization of solid state fermentation conditions for the production of cellulase by Trichoderma reesei. J Environ Biol 33:5–8

    PubMed  CAS  Google Scholar 

  • Metreveli E, Kachlishvili E, Singer SW, Elisashvili V (2017) Alteration of white-rot basidiomycetes cellulase and xylanase activities in the submerged co-cultivation and optimization of enzyme production by Irpex lacteus and Schizophyllum commune. Bioresour Technol 241:652–660. https://doi.org/10.1016/j.biortech.2017.05.148

    Article  PubMed  CAS  Google Scholar 

  • Mikiashvili N, Elisashvili V, Wasser S, Nevo E (2005) Carbon and nitrogen sources influence the ligninolytic enzyme activity of Trametes versicolor. Biotechnol Lett 27:955–959. https://doi.org/10.1007/s10529-005-7662-x

    Article  PubMed  CAS  Google Scholar 

  • Mishra BK, Lata AP (2007) Lignocellulolytic enzyme production from submerged fermentation of paddy straw. Indian J Microbiol 47:176–179. https://doi.org/10.1007/s12088-007-0034-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Munk L, Sitarz AK, Kalyani DC, Mikkelsen JC, Meyer AS (2015) Can laccases catalyze bond cleavage in lignin? Biotechnol Adv 33:13–24. https://doi.org/10.1016/j.biotechadv.2014.12.008

    Article  PubMed  CAS  Google Scholar 

  • Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Berriman M, Abe K, Archer DB, Bermejo C, Bennett J, Bowyer P, Chen D, Collins M, Coulsen R, Davies R, Dyer PS, Farman M, Fedorova N, Fedorova N, Feldblyum TV, Fischer R, Fosker N, Fraser A, García JL, García MJ, Goble A, Goldman GH, Gomi K, Griffith-Jones S, Gwilliam R, Haas B, Haas H, Harris D, Horiuchi H, Huang J, Humphray S, Jiménez J, Keller N, Khouri H, Kitamoto K, Kobayashi T, Konzack S, Kulkarni R, Kumagai T, Lafon A, Latgé J-P, Li W, Lord A, Lu C, Majoros WH, May GS, Miller BL, Mohamoud Y, Molina M, Monod M, Mouyna I, Mulligan S, Murphy L, O’Neil S, Paulsen I, Peñalva MA, Pertea M, Price C, Pritchard BL, Quail MA, Rabbinowitsch E, Rawlins N, Rajandream M-A, Reichard U, Renauld H, Robson GD, Rodriguez de Córdoba S, Rodríguez-Peña JM, Ronning CM, Rutter S, Salzberg SL, Sanchez M, Sánchez-Ferrero JC, Saunders D, Seeger K, Squares R, Squares S, Takeuchi M, Tekaia F, Turner G, Vazquez de Aldana CR, Weidman J, White O, Woodward J, Yu J-H, Fraser C, Galagan JE, Asai K, Machida M, Hall N, Barrell B, Denning DW (2005) Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438:1151–1156. https://doi.org/10.1038/nature04332

    Article  PubMed  CAS  Google Scholar 

  • Ohkuma M, Maeda Y, Johjima T, Kudo T (2001) Lignin degradation and roles of white rot fungi: study on an efficient symbiotic system in fungus-growing termites and its application to bioremediation. Microbiology 42:39–42

    CAS  Google Scholar 

  • Ohm RA, de Jong JF, Lugones LG, Aerts A, Kothe E, Stajich JE, de Vries RP, Record E, Levasseur A, Baker SE, Bartholomew KA, Coutinho PM, Erdmann S, Fowler TJ, Gathman AC, Lombard V, Henrissat B, Knabe N, Kües U, Lilly WW, Lindquist E, Lucas S, Magnuson JK, Piumi F, Raudaskoski M, Salamov A, Schmutz J, Schwarze FWMR, vanKuyk PA, Horton JS, Grigoriev IV, Wösten HAB (2010) Genome sequence of the model mushroom Schizophyllum commune. Nat Biotechnol 28:957–963. https://doi.org/10.1038/nbt.1643

    Article  PubMed  CAS  Google Scholar 

  • Okereke OE, Akanya HO, Egwim EC (2017) Purification and characterization of an acidophilic cellulase from Pleurotus ostreatus and its potential for agrowastes valorization. Biocatalysis Agric Biotechnol 12:253–259. https://doi.org/10.1016/j.bcab.2017.10.018

    Article  Google Scholar 

  • Oostra J, Tramper J, Rinzema A (2000) Model-based bioreactor selection for large-scale solid-state cultivation of Coniothyrium minitans spores on oats. Enzym Microb Technol 27:652–663. https://doi.org/10.1016/S0141-0229(00)00261-1

    Article  CAS  Google Scholar 

  • Orzua MC, Mussatto SI, Contreras-Esquivel JC, Rodriguez R, de la Garza H, Teixeira JA, Aguilar CN (2009) Exploitation of agro industrial wastes as immobilization carrier for solid-state fermentation. Ind Crop Prod 30:24–27. https://doi.org/10.1016/j.indcrop.2009.02.001

    Article  CAS  Google Scholar 

  • Pandey A (2003) Solid-state fermentation. Biochem Eng J 13:81–84. https://doi.org/10.1016/S1369-703X(02)00121-3

    Article  CAS  Google Scholar 

  • Papagianni M (2004) Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol Adv 22:189–259. https://doi.org/10.1016/j.biotechadv.2003.09.005

    Article  PubMed  CAS  Google Scholar 

  • Pedri ZC, Lozano LMS, Hermann KL, Helm CV, Peralta RM, Tavares LBB (2015) Influence of nitrogen sources on the enzymatic activity and grown by Lentinula edodes in biomass Eucalyptus benthamii. Braz J Biol 75:940–947. https://doi.org/10.1590/1519-6984.03214

    Article  PubMed  CAS  Google Scholar 

  • Pereira BMP, Alvarez TM, da Silva DP, Dillon AJP, Squina FM, da Cruz Pradella JG (2013) Cellulase on-site production from sugar cane bagasse using Penicillium echinulatum. Bioenergy Res 6:1052–1062. https://doi.org/10.1007/s12155-013-9340-5

    Article  CAS  Google Scholar 

  • Philippoussis A, Diamantopoulou P (2011) Agro-food industry wastes and agricultural residues conversion into high value products by mushroom cultivation. In Proceedings of the 7th International conference on mushroom biology and mushroom products (ICMBMP7), France 339–351

  • Pierce BC, Agger JW, Wichmann J, Meyer AS (2017) Oxidative cleavage and hydrolytic boosting of cellulose in soybean spent flakes by Trichoderma reesei Cel61A lytic polysaccharide monooxygenase. Enzym Microb Technol 98:58–66. https://doi.org/10.1016/j.enzmictec.2016.12.007

    Article  CAS  Google Scholar 

  • Quinlan RJ, Sweeney MD, Lo Leggio L, Otten H, Poulsen J-CN, Johansen KS, Krogh KBRM, Jørgensen CI, Tovborg M, Anthonsen A, Tryfona T, Walter CP, Dupree P, Xu F, Davies GJ, Walton PH (2011) Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci U S A 108:15079–15084. https://doi.org/10.1073/pnas.1105776108

    Article  PubMed  PubMed Central  Google Scholar 

  • Riley R, Salamov AA, Brown W, Nagy LG, Floudas D, Held BW, Levasseur A, Lombard V, Morin E, Lindquist EA, Sun H, Labutti KM, Jabbour D, Luo H, Baker SE, Antonio G, Walton JD, Blanchette RA, Martin F, Cullen D, Hibbett DS, Riley R, Salamov AA, Brown DW, Nagy LG, Floudas D, Held BW (2014) Correction for Riley et al., Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci 111:14959–14959. https://doi.org/10.1073/pnas.1418116111

    Article  CAS  Google Scholar 

  • Rytioja J, Hildén K, Yuzon J, Hatakka A, de Vries RP, Mäkelä MR (2014) Plant-polysaccharide-degrading enzymes from basidiomycetes. Microbiol Mol Biol Rev 78:614–649. https://doi.org/10.1128/MMBR.00035-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Saha BC, Kennedy GJ, Qureshi N, Cotta MA (2017) Biological pretreatment of corn stover with Phlebia brevispora NRRL-13108 for enhanced enzymatic hydrolysis and efficient ethanol production. Biotechnol Prog 33:365–374. https://doi.org/10.1002/btpr.2420

    Article  PubMed  CAS  Google Scholar 

  • Saratale GD, Kshirsagar SD, Sampange VT, Saratale RG, Oh SE, Govindwar SP, Oh MK (2014) Cellulolytic enzymes production by utilizing agricultural wastes under solid state fermentation and its application for biohydrogen production. Appl Biochem Biotechnol 174:2801–2817. https://doi.org/10.1007/s12010-014-1227-1

    Article  PubMed  CAS  Google Scholar 

  • Sasidhara R, Thirunalasundari T (2014) Lignolytic and lignocellulosic enzymes of Ganoderma lucidum in liquid medium. Eur J Exp Biol 4:375–379

    Google Scholar 

  • Sergentani AG, Gonou-Zagou Z, Kapsanaki-Gotsi E, Hatzinikolaou DG (2016) Lignocellulose degradation potential of Basidiomycota from Thrace (NE Greece). Int Biodeterior Biodegradation 114:268–277. https://doi.org/10.1016/j.ibiod.2016.07.004

    Article  CAS  Google Scholar 

  • Sharma D, Sud A, Bansal S, Mahajan R, Sharma BM, Chauhan RS, Goel G (2018) Endocellulase production by Cotylidia pannosa and its application in saccharification of wheat bran to bioethanol. BioEnergy Res 11:219–227. https://doi.org/10.1007/s12155-017-9890-z

    Article  Google Scholar 

  • Singhania RR, Patel AK, Sukumaran RK, Larroche C, Pandey A (2013) Role and significance of beta-glucosidases in the hydrolysis of cellulose for bioethanol production. Bioresour Technol 127:500–507. https://doi.org/10.1016/j.biortech.2012.09.012

    Article  PubMed  CAS  Google Scholar 

  • Sørensen A, Teller PJ, Lübeck PS, Ahring BK (2011) Onsite enzyme production during bioethanol production from biomass: screening for suitable fungal strains. Appl Biochem Biotechnol 164:1058–1070. https://doi.org/10.1007/s12010-011-9194-2

    Article  PubMed  CAS  Google Scholar 

  • Suzuki H, MacDonald J, Syed K, Salamov A, Hori C, Aerts A, Henrissat B, Wiebenga A, VanKuyk PA, Barry K, Lindquist E, LaButti K, Lapidus A, Lucas S, Coutinho P, Gong Y, Samejima M, Mahadevan R, Abou-Zaid M, de Vries RP, Igarashi K, Yadav JS, Grigoriev IV, Master ER (2012) Comparative genomics of the white-rot fungi, Phanerochaete carnosa and P. chrysosporium, to elucidate the genetic basis of the distinct wood types they colonize. BMC Genomics 13:444. https://doi.org/10.1186/1471-2164-13-444

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tsai SL, Park M, Chen W (2013) Size-modulated synergy of cellulase clustering for enhanced cellulose hydrolysis. Biotechnol J 8:257–261. https://doi.org/10.1002/biot.201100503

    Article  PubMed  CAS  Google Scholar 

  • Valadares F, Gonçalves TA, Gonçalves DSPO, Segato F, Romanel E, Milagres AMF, Squina FM, Ferraz A (2016) Exploring glycoside hydrolases and accessory proteins from wood decay fungi to enhance sugarcane bagasse saccharification. Biotechnol Biofuels 9:110. https://doi.org/10.1186/s13068-016-0525-y

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Valášková V, Baldrian P (2006) Estimation of bound and free fractions of lignocellulose-degrading enzymes of wood-rotting fungi Pleurotus ostreatus, Trametes versicolor and Piptoporus betulinus. Res Microbiol 157:119–124. https://doi.org/10.1016/j.resmic.2005.06.004

    Article  PubMed  CAS  Google Scholar 

  • Wanzenböck E, Apprich S, Tirpanalan Ö, Zitz U, Kracher D, Schedle K, Kneifel W (2017) Wheat bran biodegradation by edible Pleurotus fungi—sustainable perspective for food and feed. LWT-Food Sci Technol 86:123–131. https://doi.org/10.1016/j.lwt.2017.07.051

    Article  CAS  Google Scholar 

  • Xiao LP, Shi ZJ, Bai YY, Wang W, Zhang XM, Sun RC (2013) Biodegradation of lignocellulose by white-rot fungi: structural characterization of water-soluble hemicelluloses. Bioenergy Res 6:1154–1164. https://doi.org/10.1007/s12155-013-9302-y

    Article  CAS  Google Scholar 

  • Xu C, Ma F, Zhang X (2009) Lignocellulose degradation and enzyme production by Irpex lacteus CD2 during solid-state fermentation of corn stover. J Biosci Bioeng 108:372–375. https://doi.org/10.1016/j.jbiosc.2009.04.023

    Article  PubMed  CAS  Google Scholar 

  • Yoon LW, Ang TN, Ngoh GC, Chua ASM (2014) Fungal solid-state fermentation and various methods of enhancement in cellulase production. Biomass Bioenergy 67:319–338. https://doi.org/10.1016/j.biombioe.2014.05.013

    Article  CAS  Google Scholar 

  • Zhang Y-HP, Himmel ME, Mielenz JR (2006) Outlook for cellulase improvement: screening and selection strategies. Biotechnol Adv 24:452–481. https://doi.org/10.1016/j.biotechadv.2006.03.003

    Article  CAS  Google Scholar 

  • Zhou S, Herpoël-Gimbert I, Grisel S, Sigoillot JC, Sergent M, Raouche S (2018) Biological wheat straw valorization: multicriteria optimization of Polyporus brumalis pretreatment in packed bed bioreactor. MicrobiologyOpen 7:e530

    Article  CAS  Google Scholar 

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Funding

This study was funded by the DANIDA Fellowship Centre via the Second Generation Bioenergy Project (2GBIONRG DFC no. 10-018RISØ).

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Authors and Affiliations

  1. Department of Chemical and Biochemical Engineering, Center for Bioprocess Engineering, Technical University of Denmark, Lyngby, Denmark

    Joseph A. Bentil, Anders Thygesen, Lene Lange & Anne S. Meyer

  2. Department of Chemical Engineering, College of Engineering, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana

    Moses Mensah

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  1. Joseph A. Bentil
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  2. Anders Thygesen
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  3. Moses Mensah
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  4. Lene Lange
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Correspondence to Anne S. Meyer.

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Bentil, J.A., Thygesen, A., Mensah, M. et al. Cellulase production by white-rot basidiomycetous fungi: solid-state versus submerged cultivation. Appl Microbiol Biotechnol 102, 5827–5839 (2018). https://doi.org/10.1007/s00253-018-9072-8

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  • DOI: https://doi.org/10.1007/s00253-018-9072-8

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