Abstract
Laccases (E.C. 1.10.3.2) produced by white-rot fungi (WRF) can be widely used, but the high cost prevents their use in large-scale industrial processes. Finding a solution to the problem could involve laccase production by solid-state fermentation (SSF) simulating the natural growth conditions for WRF. SSF offers several advantages over conventional submerged fermentation (SmF), such as higher efficiency and productivity of the process and pollution reduction. The aim of this review is therefore to provide an overview of the current state of knowledge about the laccase production by WRF under SSF conditions. The focus is on variations in the up-stream process, fermentation and down-stream process and their impact on laccase activity. The variations of up-stream processing involve inoculum preparation, inoculation of the medium and formulation of the propagation and production media. According to the studies, the production process can be shortened to 5–7 days by the selection of a suitable combination of lignocellulosic material and laccase producer without the need for any additional components of the culture medium. Efficient laccase production was achieved by valorisation of wastes as agro-food, municipal wastes or waste generated from wood processing industries. This leads to a reduction of costs and an increase in competitiveness compared to other commonly used methods and/or procedures. There will be significant challenges and opportunities in the future, where SSF could become more efficient and bring the enzyme production to a higher level, especially in new biorefineries, bioreactors and biomolecular/genetic engineering.
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Abbreviations
- ABTS:
-
2,2′-Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid)
- ATPE:
-
Aqueous two-phase extraction
- BOD:
-
Biological oxygen demand
- COD:
-
Chemical oxygen demand
- DMP:
-
2,6-Dimethoxyphenol
- d.r.:
-
Dry residue
- d.s.:
-
Dry substrate
- gfs:
-
Number of units of enzyme produced from 5 g fermented substrate
- hum.:
-
Humidity
- Met:
-
Methylene
- NHE:
-
Normal hydrogen electrode
- PMSF:
-
Phenylmethanesulfonyl fluoride
- R.T.:
-
Room temperature
- SE:
-
Steam explosion
- SmF:
-
Submerged fermentation
- SSF:
-
Solid-state fermentation
- T:
-
Temperature
- TPP:
-
Three-phase partitioning
- VA:
-
Veratryl alcohol
- WRF:
-
White-rot fungi
- XYL:
-
2,5-Xylidine
References
Adekunle AE, Zhang C, Guo C, Liu CZ (2017) Laccase production from Trametes versicolor in solid-state fermentation of steam-exploded pretreated corn stalk. Waste Biomass Valori 8:153–159. https://doi.org/10.1007/s12649-016-9562-9
Akpinar M, Urek RO (2017) Induction of fungal laccase production under solid state bioprocessing of new agroindustrial waste and its application on dye decolorization. 3 Biotech 7(2):98. https://doi.org/10.1007/s13205-017-0742-5
Amin FR, Khalid H, Zhang H, Rahman S, Zhang R, Liu G, Chen C (2017) Pretreatment methods of lignocellulosic biomass for anaerobic digestion. AMB Express 7:72. https://doi.org/10.1186/s13568-017-0375-4
Andriani A, Sukorini A, Perwitasari U, Yopi (2019) Enhancement of laccase production in a new isolated Trametes hirsuta LBF-AA017 by lignocellulosic materials and its application for removal of chemical dyes. IOP Conf Ser Earth Environ Sci 308(1):012015. https://doi.org/10.1088/1755-1315/308/1/012015
Antecka A, Blatkiewicz M, Boruta T, Górak A, Ledakowicz S (2019) Comparison of downstream processing methods in purification of highly active laccase. Bioprocess Biosyst Eng 42:1635–1645. https://doi.org/10.1007/s00449-019-02160-3
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
Asemoloye MD, Marchisio MA, Gupta VK, Pecoraro L (2021) Genome-based engineering of ligninolytic enzymes in fungi. Microb Cell Fact 20:20. https://doi.org/10.1186/s12934-021-01510-9
Aydinoğlu T, Sargin S (2013) Production of laccase from Trametes versicolor by solid-state fermentation using olive leaves as a phenolic substrate. Bioprocess Biosyst Eng 36(2):215–222. https://doi.org/10.1007/s00449-012-0777-2
Babu RC, Ketanapalli H, Beebi SK, Kolluruu VC (2018) Wheat bran-composition and nutritional quality: a review. Adv Appl Microbiol 9(1):555754. https://doi.org/10.19080/AIBM.2018.09.555754
Baldrian P (2003) Interaction of heavy metals with white-rot fungi. Enzyme Microb Technol 32(1):78–91. https://doi.org/10.1016/S0141-0229(02)00245-4
Barreto JAR, Anaguano AH (2014) Evaluation of growth and compatibility of white rot fungi. Ciencia En Desarrollo 5(2):197–205
Bautista EG, Gutierrez E, Dupuy N, Gaime-Perraud I, Ziarelli F, da Silva AMF (2019) Pre-treatment of a sugarcane bagasse-based substrate prior to saccharification: effect of coffee pulp and urea on laccase and cellulase activities of Pycnoporus sanguineus. J Environ Manage 239:178–186. https://doi.org/10.1016/j.jenvman.2019.03.033
Bettin F, Cousseau F, Martins K, Boff NA, Zaccaria S, da Silveira MM, Dillon AJP (2019) Phenol removal by laccases and other phenol oxidases of Pleurotus sajor-caju PS-2001 in submerged cultivations and aqueous mixtures. J Environ Manage 236:581–590. https://doi.org/10.1016/j.jenvman.2019.02.011
Bilal M, Noreen S, Asgher M, Parveen S (2021) Development and characterization of cross-linked laccase aggregates (Lac-CLEAs) from Trametes versicolor IBL-04 as eco-friendly biocatalyst for degradation of dye-based environmental pollutants. Environ Technol Innov 21:101364. https://doi.org/10.1016/j.eti.2021.101364
Blatkiewicz M, Antecka A, Górak A, Ledakowicz S (2017) Laccase concentration by foam fractionation of Cerrena unicolor and Pleurotus sapidus culture supernatants. Chem Process Eng 38(3):455–464. https://doi.org/10.1515/cpe-2017-0035
Blatkiewicz M, Antecka A, Boruta T, Górak A, Ledakowicz S (2018) Partitioning of Cerrena unicolor and Pleurotus sapidus laccases in polyethylene glycol-phosphate aqueous two-phase systems. Process Biochem 67:165–174. https://doi.org/10.1016/j.procbio.2018.01.011
Boran F, Yesilada O (2011) Enhanced production of laccase by fungi under solid substrate fermentation condition. BioResources 6(4):4404–4416
Borràs E, Llorens-Blanch G, Rodríguez-Rodríguez CE, Sarrà M, Caminal G (2011) Soil colonization by Trametes versicolor grown on lignocellulosic materials: substrate selection and naproxen degradation. Int Biodeterior Biodegrad 65(6):846–852. https://doi.org/10.1016/j.ibiod.2011.06.005
Chauhan R (2019) Nitrogen sources and trace elements influence laccase and peroxidase enzymes activity of Grammothele fuligo. Vegetos 32:316–323. https://doi.org/10.1007/s42535-019-00049-w
Chenthamarakshan A, Parambayil N, Miziriya N, Soumya PS, Lakshmi MSK, Ramogopal A, Dileep A, Nambisan P (2017) Optimization of laccase production from Marasmiellus palmivorus LA1 by Taguchi method of design of experiments. BMC Biotechnol 17:12. https://doi.org/10.1186/s12896-017-0333-x
Chmelová D, Ondrejovič M (2015) Effect of metal ions on triphenylmethane dye decolorization by laccase from Trametes versicolor. Nova Biotechnol Chim 14(2):191–200. https://doi.org/10.1515/nbec-2015-0026
Chmelová D, Ondrejovič M (2016) Purification and characterization of extracellular laccase produced by Ceriporiopsis subvermispora and decolorization of triphenylmethane dyes. J Basic Microbiol 56(11):1173–1182. https://doi.org/10.1002/jobm.201600152
Claus H (2003) Laccases and their occurrence in prokaryotes. Arch Microbiol 179(3):145–150. https://doi.org/10.1007/s00203-002-0510-7
Coconi-Linares N, Ortiz-Vázquez E, Fernández F, Loske AM, Gómez-Lim MA (2015) Recombinant expression of four oxidoreductases in Phanerochaete chrysosporium improves degradation of phenolic and non-phenolic substrates. J Biotechnol 209:76–84. https://doi.org/10.1016/j.jbiotec.2015.06.401
Dennison C, Lovrien R (1997) Three phase partitioning: concentration and purification of proteins. Protein Expr Purif 11(2):149–161. https://doi.org/10.1006/prep.1997.0779
Dong XQ, Yang JS, Zhu N, Wang ET, Yuan HL (2013) Sugarcane bagasse degradation and characterization of three white-rot fungi. Bioresour Technol 131:443–451. https://doi.org/10.1016/j.biortech.2012.12.182
Dos Santos Bazanella GC, 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 (praha) 58(6):641–647. https://doi.org/10.1007/s12223-013-0253-7
Eggert C, Temp U, Eriksson KE (1996) The ligninolytic system of the white rot fungus Pycnoporus cinnabarinus: purification and characterization of the laccase. Appl Environ Microbiol 62(4):1151–1158. https://doi.org/10.1128/aem.62.4.1151-1158.1996
El-Batal AI, El-Kenawy NM, Yassin AS, Amin MA (2014) Laccase production by Pleurotus ostreatus and its application in synthesis of gold nanoparticles. Biotechnol Rep (amst) 5:31–39. https://doi.org/10.1016/j.btre.2014.11.001
Elisashvili V, Kachlishvili E, Penninckx M (2008) Effect of growth substrate, method of fermentation, and nitrogen source on lignocellulose-degrading enzymes production by white-rot basidiomycetes. J Ind Microbiol Biotechnol 35(11):1531–1538. https://doi.org/10.1007/s10295-008-0454-2
Ergun OS, Urek RO (2017) Production of ligninolytic enzymes by solid state fermentation using Pleurotus ostreatus. Ann Agrar Sci 15(2):273–277. https://doi.org/10.1016/j.aasci.2017.04.003
Fakoussa RM, Frost PJ (1999) In vivo-decolorization of coal-derived humic acids by laccase-excreting fungus Trametes versicolor. App Microbiol Biotechnol 52:60–65. https://doi.org/10.1007/s002530051487
Fenice M, Sermanni GG, Federici F, D’Annibale A (2003) Submerged and solid-state production of laccase and Mn-peroxidase by Panus tigrinus on olive mill wastewater-based media. J Biotechnol 100(1):77–85. https://doi.org/10.1016/S0168-1656(02)00241-9
Ferreira RDG, Azzoni AR, Freitas S (2018) Techno-economic analysis of the industrial production of low-cost enzyme using E. coli: the case of recombinant β-glucosidase. Biotechnol Biofuels 11:81. https://doi.org/10.1186/s13068-018-1077-0
Fletcher I, Freer A, Ahmed A, Fitzgerald P (2019) Effect of temperature and growth media on mycelium growth of Pleurotus ostreatus and Ganoderma lucidum strains. Cohesive J Microbiol Infect Dis. https://doi.org/10.31031/CJMI.2019.02.000549
Freitag M, Morell JJ (1992) Decolorization of the polymeric dye poly R-478 by wood-inhabiting fungi. Can J Microbiol 38(8):811–822. https://doi.org/10.1139/m92-133
Gabdulkhakov A, Kolyadenko I, Kostareva O, Mikhaylina A, Oliveira P, Tamagnini P, Lisov A, Tishchenko S (2019) Investigation of accessibility of T2/T3 copper center of two domain laccase from Streptomyces griseoflavus Ac-993. Int J Mol Sci 20(13):3184. https://doi.org/10.3390/ijms20133184
Garzillo AM, Colao MC, Buonocore V, Oliva R, Falcigno L, Saviano M, Santoro AM, Zappala R, Bonomo RF, Bianco C, Giardina P, Palmieri G, Sannia G (2001) Structural and kinetic characterization of native laccases from Pleurotus ostreatus, Rigidoporus lignosus, and Trametes trogii. J Protein Chem 20(3):191–201. https://doi.org/10.1023/A:1010954812955
Gassara F, Brar SK, Tyagi RD, John RP, Verma M, Valero JR (2011) Parameter optimization for production of ligninolytic enzymes using agro-industrial wastes by response surface method. Biotechnol Bioprocess Eng 16:343–351. https://doi.org/10.1007/s12257-010-0264-z
Hafid HS, Baharuddin AS, Mokhtar MN, Omar FN, Mohammed MAP, Wakisaka M (2021) Enhanced laccase production for oil palm biomass delignification using biological pretreatment and its estimation at biorafinary scale. Biomas Bioenerg 144:105904. https://doi.org/10.1016/j.biombioe.2020.105904
Hariharan S, Nambisan P (2013) Optimization of lignin peroxidase, manganese peroxidase, and lac production from Ganoderma lucidum under solid state fermentation of pineapple leaf. BioResources 8(1):250–271. https://doi.org/10.15376/biores.8.1.250-271
Hazuchová M, Chmelová D, Ondrejovič M (2017) The optimization of propagation medium for the increase of laccase production by the white-rot fungus Pleurotus ostreatus. Nova Biotechnol Chim 16(2):113–123. https://doi.org/10.1515/nbec-2017-0016
Hoa HT, Wang C-L (2014) The effects of temperature and nutritional conditions on mycelium growth of two oyster mushrooms (Pleurotus ostreatus and Pleurotus cystidiosus). Mycobiol 43(1):14–23. https://doi.org/10.5941/MYCO.2015.43.1.14
Huang S, Huang D, Wu Q, Hou M, Tang X, Zhou J (2020) Effect of environmental C/N ratio on activities of lignin-degrading enzymes produced by Phanerochaete chrysosporium. Pedosphere 30(2):285–292. https://doi.org/10.1016/S1002-0160(17)60391-6
Iark D, Buzzo AJR, Garcia JAA, Côrrea VG, Helm CV, Côrrea RCG, Peralta RA, Moreira RFPM, Bracht A, Peralta RM (2019) Enzymatic degradation and detoxification of azo dye Congo red by a new laccase from Oudemansiella canarii. Bioresour Technol 289:121655. https://doi.org/10.1016/j.biortech.2019.121655
Iqbal M, Tao Y, Xie S, Zhu Y, Chen D, Wang X, Huang L, Peng D, Sattar A, Shabbir MAB, Hussain HI, Ahmed S, Yuan Z (2016) Aqueous two-phase system (ATPS): an overview and advances in its applications. Biol Proced Online 18:18. https://doi.org/10.1186/s12575-016-0048-8
Janusz G, Kucharzyk KH, Pawlik A, Staszczak M, Paszczynski AJ (2013) Fungal laccase, manganese peroxidase and lignin peroxidase: gene expression and regulation. Enzyme Microb Technol 52(1):1–12. https://doi.org/10.1016/j.enzmictec.2012.10.003
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(4):391–397. https://doi.org/10.1007/s11274-005-9046-8
Kamei I, Hirota Y, Maguro S (2012) Integrated delignification and simultaneous saccharification and fermentation of hard wood by a white-rot fungus, Phlebia sp. MG-60. Bioresour Technol 126:137–141. https://doi.org/10.1016/j.biortech.2012.09.007
Karp SG, Faraco V, Amore A, Birolo L, Giangrande C, Soccol T, Pandey A, Soccol CR (2012) Characterization of laccase isoforms produced by Pleurotus ostreatus in solid state fermentation of sugarcane bagasse. Bioresour Technol 114:735–739. https://doi.org/10.1016/j.biortech.2012.03.058
Karp SG, Faraco V, Amore A, Letti LAJ, Soccol VT, Soccol CR (2015) Statistical optimization of laccase production and delignification of sugarcane bagasse by Pleurotus ostreatus in solid-state fermentation. BioMed Res Int 2015:181204. https://doi.org/10.1155/2015/181204
Kim Y, Nicell JA (2006) Impact of reaction conditions on the laccase catalyzed conversion of bisphenol A. Bioresour Technol 97(12):1431–1442. https://doi.org/10.1016/j.biortech.2005.06.017
Koutrotsios G, Larou E, Mountzouris KC, Zervakis GI (2016) Detoxification of olive mill wastewater and bioconversion of olive crop residues into high-value-added biomass by the choice edible mushroom Hericium erinaceus. Appl Biochem Biotechnol 180:195–209. https://doi.org/10.1007/s12010-016-2093-9
Krishna C (2005) Solid-state fermentation systems—an overview. Crit Rev Biotechnol 25(1–2):1–30. https://doi.org/10.1080/07388550590925383
Krumova E, Kostadinova N, Miteva-Staleva J, Stoyancheva G, Spassova B, Abrashev R, Angelova M (2018) Potential of ligninolytic enzymatic complex produced by white-rot fungi from genus Trametes isolated from Bulgarian forest soil. Eng Life Sci 18(9):692–701. https://doi.org/10.1002/elsc.201800055
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 Biodeterior Biodegrad 104:238–243. https://doi.org/10.1016/j.ibiod.2015.06.017
Kumar V, Sathyaselvabala V, Kirupha SD, Murugesan A, Vidyadevi T, Sivanesan S (2011) Application of response surface methodology to optimize three phase partitioning for purification of laccase from Pleurotus ostreatus. Sep Sci Technol 46(12):1922–1930. https://doi.org/10.1080/01496395.2011.583306
Kumaran S, Sastry CA, Vikineswary S (1997) Laccase, cellulase and xylanase activities during growth of Pleurotus sajor-caju on sago hampas. World J Microbiol Biotechnol 13(1):43–49. https://doi.org/10.1007/BF02770806
Kunstová J, Legerská B, Lipničanová S, Chmelová D, Ondrejovič M (2020) The effect of the repeated extraction on laccases produced by the white-rot fungus Pleurotus ostreatus under solid-state cultivation. Quaere 2020—Hradec Králové: Magnanimitas akademické sdružení, pp 456–462. ISBN 978-80-87952-32-0
Legerská B, Chmelová D, Ondrejovič M (2016) Degradation of synthetic dyes by laccases—a mini-review. Nova Biotechnol Chim 15(1):90–106. https://doi.org/10.1515/nbec-2016-0010
Legerská B, Chmelová D, Ondrejovič M (2018a) Azonaphthalene dyes decolorization and detoxification by laccase from Trametes versicolor. Nova Biotechnol Chim 17(2):172–180. https://doi.org/10.2478/nbec-2018-0018
Legerská B, Chmelová D, Ondrejovič M (2018b) Decolourization and detoxification of monoazo dyes by laccase from the white-rot fungus Trametes versicolor. J Biotechnol 285:84–90. https://doi.org/10.1016/j.jbiotec.2018.08.011
Leite P, Sousa D, Fernandes H, Ferreira M, Costa AR, Filipe D, Gonçalves M, Peres H, Belo I, Salgado JM (2021) Recent advances in production of lignocellulolytic enzymes by solid-state fermentation of agro-industrial waste. Curr Opin Green Suitain Chem 27:100407. https://doi.org/10.1016/j.cogsc.2020.100407
Levasseur A, Lomascolo A, Chabrol O, Ruiz-Dueñas FJ, Boukhris-Uzan E, Piumi F, Kües U, Ram AFJ, Murat C, Haon M, Benoit I, Arfi Y, Chevret D, Drula E, Kwon MJ, Gouret P, Lesage-Meessen L, Lombard V, Mariette J, Noirot C, Park J, Patyshakuliyeva A, Sigoillot JC, Wiebenga A, Wösten HAB, Martin F, Coutinho FP, de Vries RP, Martínez AT, Klopp C, Pontarotti P, Henrissat B, Record E (2014) The genome of the white-rot fungus Pycnoporus cinnabarinus: a basidiomycete model with a versatile arsenal for lignocellulosic biomass breakdown. BMC Genomics 15:486. https://doi.org/10.1186/1471-2164-15-486
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(1):207–214. https://doi.org/10.1016/j.bej.2007.09.004
Li K, Xu F, Eriksson KEL (1999) Comparison of fungal laccases and redox mediators in oxidation of a nonphenolic lignin model compound. Appl Environ Microbiol 65(6):2654–2660. https://doi.org/10.1128/AEM.65.6.2654-2660.1999
Liu Y, Yan M, Huang J (2015) Three-phase partitioning for purification of laccase produced by Coriolopsis trogii under solid fermentation. Am J Food Technol 10(3):127–134. https://doi.org/10.3923/ajft.2015.127.134
Liu J, Wang Z, Li H, Hu C, Raymer P, Huang Q (2018) Effect of solid-state fermentation of peanut shell on its dye adsorption performance. Bioresour Technol 249:307–314. https://doi.org/10.1016/j.biortech.2017.10.010
Liu SH, Tsai SL, Gou PY, Lin CW (2020) Inducing laccase activity in white rot fungi using copper ions and improving the efficiency of azo dye treatment with electricity generation using microbial fuel cells. Chemosphere 243:125304. https://doi.org/10.1016/j.chemosphere.2019.125304
Lorenzo M, Moldes D, Rodríguez Couto S, Sanromán A (2002) Improving laccase production by employing different lignocellulosic wastes in submerged cultures of Trametes versicolor. Bioresour Technol 82(2):109–113. https://doi.org/10.1016/S0960-8524(01)00176-6
Lowe CR, Lowe AR, Gupta G (2001) New developments in affinity chromatography with potential application in the production of biopharmaceuticals. J Biochem Biophys Methods 49(1–3):561–574. https://doi.org/10.1016/s0165-022x(01)00220-2
Machczynsky MC, Vijgenboom E, Samym B, Canters GW (2004) Characterization of SLAC: a small laccase from Streptomyces coelicolor with unprecedented activity. Protein Sci 13(9):2388–2397. https://doi.org/10.1110/ps.04759104
Mata G, Murrieta Hernández DM, Andreu LGI (2005) Changes in lignocellulolytic enzyme activities in six Pleurotus spp. strains cultivated on coffee pulp in confrontation with Trichoderma spp. World J Microbiol Biotechnol 21(2):143–150. https://doi.org/10.1007/s11274-004-3041-3
Mazumder S, Basu SK, Mukherjee M (2009) Laccase production in solid-state and submerged fermentation of Pleurotus ostreatus. Eng Life Sci 9(1):45–52. https://doi.org/10.1002/elsc.200700039
Messerschmidt A (1997) Spatial structures of ascorbate oxidase, laccase and related proteins: implications for the catalytic mechanism. In: Messerschmidt A (ed) Multi-copper oxidases. World Scientific, Singapore, pp 23–80
Minussi RC, Durán PGM, N, (2007) Laccase induction in fungi and laccase/N-OH mediator system applied in paper mill effluent. Bioresour Technol 98(1):158–164. https://doi.org/10.1016/j.biortech.2005.11.008
Mishra A, Kumar S (2007) Cyanobacterial biomass as N-supplement to agro-waste for hyper-production of laccase from Pleurotus ostreatus in solid state fermentation. Process Biochem 42(4):681–685. https://doi.org/10.1016/j.procbio.2006.09.022
Moldes D, Gallego PP, Rodríguez Couto S, Sandromán A (2003) Grape seeds: the best lignocellulosic waste to produce laccase by solid state cultures of Trametes hirsuta. Biotechnol Lett 25:491–495. https://doi.org/10.1023/A:1022660230653
Montoya S, Patiño A, Sánchez ÓJ (2021) Production of lignocellulolytic enzymes and biomass of Trametes versicolor from agro-industrial residues in a novel fixed-bed bioreactor with natural convection and forced aeration at pilot scale. Processes 9(2):397. https://doi.org/10.3390/pr9020397
Mushtaq M, Iqbal MK, Khalid A, Khan RA (2018) Humification of poultry waste and rice husk using additives and its application. Int J Recycl Org Waste Agric 8:15–22. https://doi.org/10.1007/s40093-018-0224-8
Naidu Y, Siddiqui Y, Seman Idris A (2020) Comprehensive studies on optimization of ligno-hemicellulolytic enzymes by indigenous white rot hymenomycetes under solid-state cultivation using agro-industrial wastes. J Environ Manage 259:110056. https://doi.org/10.1016/j.jenvman.2019.110056
Nandal P, Ravella SP, Kuhad RC (2013) Laccase production by Coriolopsis caperata RCK2011: Optimization under solid state fermentation by Taguchi DOE methodology. Sci Rep 3:1386. https://doi.org/10.1038/srep01386
Neifar M, Jaouani A, Ellouze-Ghorbel R, Ellouze-Chaabouni S, Penninckx MJ (2009) Effect of culturing processes and copper addition on laccase production by the white-rot fungus Fomes fomentarius MUCL 35117. Lett Appl Microbiol 49(1):73–78. https://doi.org/10.1111/j.1472-765X.2009.02621.x
Neifar M, Kamoun A, Jaouani A, Ellouze-Ghorbel R, Ellouze-Chaabouni S (2011) Application of asymetrical and hoke designs for optimization of laccase production by the white-rot fungus Fomes fomentarius in solid-state fermentation. Enzyme Res 2011:368525. https://doi.org/10.4061/2011/368525
Niladevi KN, Sukumaran RK, Prema P (2007) Utilization of rice straw for laccase production by Streptomyces psammoticus in solid-state fermentation. J Ind Microbiol Biotechnol 34(10):665–674. https://doi.org/10.1007/s10295-007-0239-z
Ooijkaas LP, Weber FJ, Buitelaar RM, Tramper J, Rinzema A (2000) Defined media and inert supports: their potential as solid-state fermentation production systems. Trends Biotechnol 18(8):356–360. https://doi.org/10.1016/S0167-7799(00)01466-9
Palmieri G, Giardina P, Bianco C, Fontanella B, Sannia G (2000) Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Appl Environ Microbiol 66(3):920–924. https://doi.org/10.1128/aem.66.3.920-924.2000
Pandey A, Soccol CR, Mitchell D (2000) New developments in solid state fermentation: I-bioprocesses and products. Process Biochem 35(10):1153–1169. https://doi.org/10.1016/S0032-9592(00)00152-7
Patel H, Gupte A (2016) Optimization of different culture conditions for enhanced laccase production and its purification from Tricholoma giganteum AGHP. Bioresour Bioprocess 3:11. https://doi.org/10.1186/s40643-016-0088-6
Patel H, Gupte A, Gupte S (2009) Effect of different culture conditions and inducers on production of laccase by a basidiomycete fungal isolate Pleurotus ostreatus HP-1 under solid state fermentation. BioResources 4(1):268–284
Pecková V, Legerská B, Chmelová D, Horník M, Ondrejovič M (2020) Comparison of efficiency for monoazo dye removal by different species of white-rot fungi. Int J Environ Sci Technol 18:21–30. https://doi.org/10.1007/s13762-020-02806-w
Perdani MS, Margaretha G, Sahlan M, Hermansyah H (2019) Solid state fermentation method for production of laccase enzyme with bagasse, cornstalk and rice husk as substrates for adrenaline biosensor. Energy Rep 6(1):336–340. https://doi.org/10.1016/j.egyr.2019.08.065
Pinto PA, Fraga I, Bezerra RMF, Dias AA (2020) Phenolic and non-phenolic substrates oxidation by laccase at variable oxygen concentrations: selection of bisubstrate kinetic models from polarographic data. Biochem Eng J 153:107423. https://doi.org/10.1016/j.bej.2019.107423
Piscitelli A, Giardina P, Lettera V, Pezzella C, Sannia G, Faraco V (2011) Induction and transcriptional regulation of laccases in fungi. Curr Genomics 12(2):104–112. https://doi.org/10.2174/138920211795564331
Postemsky PD, Bidegain MA, González-Matute R, Figlas ND, Cubitto MA (2017) Pilot-scale bioconversion of rice and sunflower agro-residues into medicinal mushrooms and laccase enzymes through solid-state fermentation with Ganoderma lucidum. Bioresour Technol 231:85–93. https://doi.org/10.1016/j.biortech.2017.01.064
Prinz A, Koch K, Górak A, Zeiner T (2014) Multi-stage laccase extraction and separation using aqueous two-stage systems: experiment and model. Process Biochem 49(6):1020–1031. https://doi.org/10.1016/j.procbio.2014.03.011
Raimbault M (1998) General and microbiological aspects of solid substrate fermentation. Electron J Biotechnol 3(1):1–15. https://doi.org/10.4067/S0717-34581998000300007
Rajeeva S, Lele SS (2011) Three-phase partitioning for concentration and purification of laccase produced by submerged cultures of Ganoderma sp. WR-1. Biochem Eng J 54(2):103–110. https://doi.org/10.1016/j.bej.2011.02.006
Rangelov S, Nicell JA (2018) Modelling the transient kinetics of laccase-catalyzed oxidation of four aqueous phenolic substrates at low concentrations. Biochem Eng K 132:233–243. https://doi.org/10.1016/j.bej.2018.01.016
Revankar MS, Desai KM, Lele SS (2007) Solid-state fermentation for enhanced production of laccase using indigenously isolated Ganoderma sp. Appl Biochem Biotechnol 143(1):16–26. https://doi.org/10.1007/s12010-007-0029-0
Robinson T, McMullan G, Marchant R, Nigam P (2001) Remediation of dyes in textile effluent: a critical review on current treatment technologies with a proposed alternative. Bioresour Technol 77(3):247–255. https://doi.org/10.1016/S0960-8524(00)00080-8
Rodríguez Couto S (2012) A promising inert support for laccase production and decolouration of textile wastewater by the white-rot fungus Trametes pubescens. J Hazard Mater 233–234:158–162. https://doi.org/10.1016/j.jhazmat.2012.07.003
Rodríguez Couto S, Sanromán MA (2005) Application of solid-state fermentation to ligninolytic enzyme production. Biochem Eng J 22(3):211–219. https://doi.org/10.1016/j.bej.2004.09.013
Rodríguez Couto S, Toca-Herrera JL (2007) Laccase production at reactor scale by filamentous fungi. Biotechnol Adv 25(6):558–569. https://doi.org/10.1016/j.biotechadv.2007.07.002
Rodríguez Couto S, Gundín M, Lorenzo M, Sanromán MA (2002) Screening of supports and inducers for laccase production by Trametes versicolor in semi-solid-state conditions. Process Biochem 38(2):249–255. https://doi.org/10.1016/S0032-9592(02)00087-0
Rodríguez Couto S, Moldes D, Liébanas A, Sanromán A (2003) Investigation of several bioreactor configurations for laccase production by Trametes versicolor operating in solid-state conditions. Biochem Eng J 15(1):21–26. https://doi.org/10.1016/S1369-703X(02)00180-8
Rodríguez Couto S, Rodríguez A, Paterson RRM, Lima N, Teixeira JA (2006) Laccase activity from the fungus Trametes hirsuta using an air-lift bioreactor. Lett Appl Microbiol 42(6):612–616. https://doi.org/10.1111/j.1472-765X.2006.01879.x
Sabantina L, Kinzel F, Hauser T, Többer A, Klöcker M, Döpke C, Böttjer R, Wehlage D, Rattenholl A, Ehrmann A (2019) Comparative study of Pleurotus ostreatus mushroom grown on modified PAN nanofiber mats. Nanomaterials (basel) 9(3):475. https://doi.org/10.3390/nano9030475
Sabu A, Pandey A, Jaafar Daud M, Szakacs G (2005) Tamarind seed powder and palm kernel cake: two novel agro residues for the production of tannase under solid state fermentation by Aspergillus niger ATCC 16620. Bioresour Technol 96(11):1223–1228. https://doi.org/10.1016/j.biortech.2004.11.002
Sadeghian-Abadi S, Rezaei S, Yousefi-Mokri M, Faramarzi MA (2019) Enhanced production, one-step affinity purification, and characterization of laccase from solid-state culture of Lentinus tigrinus and delignification of pistachio shell by free and immobilized enzyme. J Environ Manage 244:235–246. https://doi.org/10.1016/j.jenvman.2019.05.058
Sardar H, Ali MA, Ayyub M, Ahmad R (2015) Effects of different culture media, temperature and pH levels on the growth of wild and exotic Pleurotus species. Pak J Phytopathol 27(2):139–145
Schneider WDH, Fontana RC, Mendonça S, Siqueira FG, Dillon AJP, Camassola M (2018) High level production of laccases and peroxidases from the newly isolated white-rot basidiomycete Marasmiellus palmivorus VE111 in a stirred-tank bioreactor in response to different carbon and nitrogen sources. Bioprocess Biochem 69:1–11. https://doi.org/10.3390/microorganisms7120665
Schulze M, Geisler L, Mejcherczyk A, Rühl M (2019) Signal peptide replacement resulted in recombinant homologous expression of laccase Lcc8 in Coprinopsis cinerea. AMB Express 9:36. https://doi.org/10.1186/s13568-019-0761-1
Šelo G, Planinić M, Tišma M, Tomas S, Komlenić DK, Bucić-Kojić A (2021) A comprehensive review on valorization of agro-food industrial residues by solid-state fermentation. Foods 10(5):927. https://doi.org/10.3390/foods10050927
Sepehri A, Sarrafhadeh M-H (2018) Effect of nutrients community on fouling mitigation and nitrification efficiency in a membrane bioreactor. Chem Eng Process: Process Intensif 128:10–18. https://doi.org/10.1016/j.cep.2018.04.006
Setiati Y, Chaidir L, Saputri A, Roosda AA (2019) Utilization of rice wastewater as an alternative medium for growth and quality of Shiitake mushrooms (Lentinula edodes). J Phys Conf Ser 1402:033034. https://doi.org/10.1088/1742-6596/1402/3/033034
Shahtahmasebi S, Pourianfar HR, Rezaeian S, Janpoor J (2017) A preliminary study on cultivation of Iranian wildgrowing medicinal mushroom Lentinus tigrinus. Int J Farming Allied Sci 6(6):149–153. https://doi.org/10.5943/cream/8/6/4
Sharma V, Jaitly AK (2017) Optimization of growth of two wild species of Pycnoporus collected from Foothill of Uttarakhand. Int J Agric Innov Res 6(1):91–94
Shleev S, Christenson A, Serezhenkov V, Burbaev D, Yaropolov A, Gorton L, Ruzgas T (2005) Electrochemical redox transformations of T1 and T2 copper sites in native Trametes hirsuta laccase at gold electrode. Biochem J 385(3):745–754. https://doi.org/10.1042/BJ20041015
Silva-Torres O, Bojorquez-Vazkuez L, Simakov A, Vazquez-Duhalt R (2019) Enhanced laccase activity of biocatalytic hybrid copper hydroxide nanocages. Enzyme Microb Technol 128:59–66. https://doi.org/10.1016/j.enzmictec.2019.05.008
Silvério SC, Rodríguez O, Tavares APM, Teixeira JA, Macedo EA (2013) Laccase recovery with aqueous two-phase systems: enzyme partitioning and stability. J Mol Catal B Enzym 87:37–43. https://doi.org/10.1016/j.molcatb.2012.10.010
Singh J, Kumar P, Saharan V, Kapoor RK (2019) Simultaneous laccase production and transformation of bisphenol-A and triclosan using Trametes versicolor. 3 Biotech 9:129. https://doi.org/10.1007/s13205-019-1648-1
Singhania RR, Patel AK, Soccol CR, Pandey A (2009) Recent advances in solid-state fermentation. Biochem Eng J 44(1):13–18. https://doi.org/10.1016/j.bej.2008.10.019
Songulashvili G, Spindler D, Jimenéz-Tobón GA, Jaspers C, Kerns G, Penninckx MJ (2015) Production of a high level of laccase by submerged fermentation at 120-L scale of Cerrena unicolor C-139 grown on wheat bran. CR Biol 338(2):121–125. https://doi.org/10.1016/j.crvi.2014.12.001
Srinivasan P, Selvankumar T, Kamala-Kannan S, Mythili R, Sengottaiyan M, Govarthanan M, Senthilkumar B, Selvam K (2019) Production and purification of laccase by Bacillus sp. using millet husks and its pesticide degradation application. 3 Biotech 9:396. https://doi.org/10.1007/s13205-019-1900-8
Stevenson L, Philips F, O´Sullivan K, Walton J, (2012) Wheat bran: its composition and benefits to health, a European perspective. Int J Food Sci Nutr 63(8):1001–1013. https://doi.org/10.3109/09637486.2012.687366
Suttisa W, Sanoamuang N (2017) Identification of Pycnoporus coccineus KKUPN1 and effect of colchicine treatment on growth and enzyme production. J Pure Appl Microbiol 11(4):1665–1673. https://doi.org/10.22207/JPAM.11.4.04
Szabo OE, Csiszar E, Toth K, Szakacs G, Koczka B (2015) Ultrasound-assisted extraction and characterization of hydrolytic and oxidative enzymes produced by solid state fermentation. Ultrason Sonochem 22:249–256. https://doi.org/10.1016/j.ultsonch.2014.07.001
Teigiserova DA, Bourgine J, Thomsen M (2021) Closing the loop of cereal waste and residues with sustainable technologies: an overview of enzyme production via fungal solid-state fermentation. Sustain Prod Concum 27:845–857. https://doi.org/10.1016/j.spc.2021.02.010
Téllez-Téllez M, Fernández JF, Montiel-González AM, Sánchez C, Díaz-Godínez G (2008) Growth and laccase production by Pleurotus ostreatus in submerged and solid-state fermentation. Appl Microbiol Biotechnol 81:675–679. https://doi.org/10.1007/s00253-008-1628-6
Tišma M, Šalić A, Planinić M, Zelić B, Potočnik M, Šelo G, Bucić-Kojić A (2020) Production, characterisation and immobilization of laccase for an efficient aniline based dye decolourization. J Water Process Eng 36:101327. https://doi.org/10.1016/j.jwpe.2020.101327
Torres-Mancera MT, Cordova-López J, Rodríguez-Serrano G, Roussos S, Ramírez-Coronel A, Favela-Torres E, Saucedo-Castañeda G (2011) Enzymatic extraction of hydroxycinnamic acids from coffee pulp. Food Technol Biotechnol 49(3):363–373
U.S. Department of Agriculture, Agricultural Research Service (2019) FoodData Central. https://fdc.nal.usda.gov. Accessed 9 Sept 2021
Velázquez L, Téllez-Téllez M, Díaz R, Bibbins-Martínez MD, Loera O, Sánchez C, Tlecuitl-Beristain S, Díaz-Godínez G (2014) Laccase isoenzymes of Pleurotus ostreatus grown at different pH in solid-state fermentation using polyurethane foam as support. Annu Res Rev Biol 4(16):2566–2578. https://doi.org/10.9734/ARRB/2014/10016
Verma P, Madamwar D (2002) Production of ligninolytic enzymes for dye decolorization by cocultivation of white-rot fungi Pleurotus ostreatus and Phanerochaete chrysosporium under solid-state fermentation. Appl Biochem Biotechnol 102:109–118. https://doi.org/10.1385/ABAB:102-103(1-6):1-6:109
Vilar DS, Fernandes CD, Nascimento VRS, Torres NH, Leite MS, Bharagava RN, Bilal M, Salazar-Banda GR, Eguiluz KIB, Ferreira LFR (2021) Hyper-production optimization of fungal oxidative green enzymes using citrus low-cost byproduct. J Environ Chem Eng 9(1):105013. https://doi.org/10.1016/j.jece.2020.105013
Vipotnik Z, Michelin M, Tavares T (2021) Development of a packed bed reactor for the removal of aromatic hydrocarbons from soil using laccase/mediator feeding system. Microbiol Res 245:126687. https://doi.org/10.1016/j.micres.2020.126687
Vonk PJ, Escobar N, Wösten HAB, Lugones LG, Ohm RA (2019) High-throughput targeted gene deletion in the model mushroom Schizophyllum commune using pre-assembled Cas9 ribonucleoproteins. Sci Rep 9:e7632. https://doi.org/10.1038/s41598-019-44133-2
Wang ZX, Liu J, Ning Y, Liao X, Jia Y (2017a) Eichhornia crassipes: agro-waster for a novel thermostable laccase production by Pycnoporus sanguineus SYBC-L1. J Biosci Bioeng 123(2):163–169. https://doi.org/10.1016/j.jbiosc.2016.09.005
Wang R, Yang J, Zhang G, Chao Y, Li Z, Ye Q, Yian S (2017b) Co-expression of beta-glucosidase and laccase in Trichoderma reesei by random insertion with enhanced filter paper activity. Mol Biotechnol 59(8):353–364. https://doi.org/10.1007/s12033-017-0018-7
Wang K-F, Guo C, Ju F, Samak NA, Zhuang G-Q, Liu C-Z (2018) Farnesol-induced hyperbranched morphology with short hyphae and bulbous tips of Coriolus versicolor. Sci Rep 8:15213. https://doi.org/10.1038/s41598-018-33435-6
Wang F, Xu L, Zhao L, Ding Z, Ma H, Terry N (2019) Fungal laccase production from lignocellulosic wastes by solid-state fermentation: a review. Microorganisms 7(12):665. https://doi.org/10.3390/microorganisms7120665
Wasak A, Drozd R, Grygorcewicz B, Jankowiak D, Rakoczy R (2018) Purification and recovery of laccase produced by submerged cultures of Trametes versicolor by three-phase partitioning as a simple and highly efficient technique. Pol J Chem Technol 20(4):88–95. https://doi.org/10.2478/pjct-2018-0059
Xie C, Gong W, Yang Q, Zhu Z, Hu Z, Peng Y (2017) White-rot fungi pretreatment combined with alkaline/oxidative pretreatment to improve enzymatic saccharification of industrial hemp. Bioresour Technol 243:188–195. https://doi.org/10.1016/j.biortech.2017.06.077
Xin F, Geng A (2011) Utilization of horticultural waste for laccase production by Trametes versicolor under solid-state fermentation. Appl Biochem Biotechnol 163(2):235–246. https://doi.org/10.1007/s12010-010-9033-x
Xu L, Sun K, Wang F, Zhao L, Hu J, Ma H, Ding Z (2020) Laccase production by Trametes versicolor in solid-state fermentation using tea residues as substrate and its application in dye decolorization. J Environ Manage 270:110904. https://doi.org/10.1016/j.jenvman.2020.110904
Yang J, Lin Q, Ng TB, Ye X, Lin J (2014) Purification and characterization of a novel laccase from Cerrena sp. HYB07 with dye decolorizing ability. PLoS ONE 9(10):e110834. https://doi.org/10.1371/journal.pone.0110834
Yang J, Wang G, Ng TB, Lin J, Ye X (2016) Laccase production and differential transcription of laccase genes in Cerrena sp. in response to metal ions, aromatic compounds, and nutrients. Front Microbiol 6:1558. https://doi.org/10.3389/fmicb.2015.01558
Yoav S, Salame TM, Feldman D, Levinson D, Ioelovich M, Morag E, Yarden O, Bayer EA, Hadar Y (2018) Effects of cre1 modification in the white-rot fungus Pleurotus ostreatus PC9: altering substrate preference during biological pretreatment. Biotechnol Biofuels 11:212. https://doi.org/10.1186/s13068-018-1209-6
Yue Q, Yang Y, Zhoa J, Zhang L, Xu L, Chu X, Liu X, Tian J, Wu N (2017) Identification of bacterial laccase cueO mutation from the metagenome of chemical plant sludge. Bioresour Bioprocess 4:48. https://doi.org/10.1186/s40643-017-0178-0
Zhang Y, Zhu Y, Liu Z, Hu S, Wang Y, Chang Y, Li R (2020) β-Cyclodextrin and ultrasound-assisted enzyme renaturation for foam fractionation of laccase from fermentation broth of Trametes hirsuta 18. J Mol Liq 298:112028. https://doi.org/10.1016/j.molliq.2019.112028
Zhou R, Fan F (2021) A comprehensive insight into the application of white rot fungi and their lignocellulolytic enzymes in the removal of organic pollutants. Sci Tot Environ 778:146132. https://doi.org/10.1016/j.scitotenv.2021.146132
Zhu X, Williamson PR (2003) A CLC-type chloride channel gene is required for laccase activity and virulence in Cryptococcus neoformans. Mol Microbiol 50(4):1271–1281. https://doi.org/10.1046/j.1365-2958.2003.03752.x
Zimbardi ALRL, Camargo PF, Carli S, Neto SA, Meleiro LP, Rosa JC, Andrade ARD, Jorge JA, Furriel RPM (2016) A high redox potential laccase from Pycnoporus sanguineus RP15: potential application for dye decolorization. Int J Mol Sci 17(5):672. https://doi.org/10.3390/ijms17050672
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This work was supported by the Slovak Research and Development Agency [Grant Number APVV-18-0154]. We thank Randy T. Legersky for checking the English in the manuscript.
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Chmelová, D., Legerská, B., Kunstová, J. et al. The production of laccases by white-rot fungi under solid-state fermentation conditions. World J Microbiol Biotechnol 38, 21 (2022). https://doi.org/10.1007/s11274-021-03207-y
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DOI: https://doi.org/10.1007/s11274-021-03207-y