Advertisement

Strategic Role of Fungal Laccases in Biodegradation of Lignin

  • Shiv Shankar
  • Shailja Singh
  • Shikha
  • Anuradha Mishra
  • Siya Ram
Chapter
Part of the Fungal Biology book series (FUNGBIO)

Abstract

Lignin is a complex organic material connecting cells, fibers, and vessels which constitute wood and other lignified components of the vascular plants. Because of its complex structure consolidated by three-dimensional cross-linking, it is highly inflexible and recalcitrant. The degradation of lignin is required for the efficient utilization of lignocellulosic biomass for the production of biofuels and other cellulose-based products. Removal of lignin is also necessary for the production of paper from wood during the process of delignification and bleaching. Existing physico-chemical methods of lignin degradation are cost and energy incentive and result in generation of toxic waste products. Biodegradation of lignin involving lignin-degrading microbes and their enzyme system is more efficient and environmentally sound approach. Biodegradation of lignin is considered as sustainable technology for the disposal of lignocellulosic biomass and its utilization for the production of value-added products. Among microbes, white rot fungi efficiently degrade lignin with the help of their oxidative extracellular ligninolytic enzymes in general and laccases (benzenediol oxygen oxidoreductase, EC 1.10.3.2) in particular. Laccases are multinuclear enzymes which effectively degrade lignin. In the presence of suitable mediators, laccases hold the potential to oxidize non-phenolic proportion of lignin and other substrates. In the backdrop of aforesaid context, this chapter is an attempt to put forth the details of role of fungal laccases and laccase mediator system in degradation of lignin.

Keywords

Lignin Biodegradation Laccases Lignocellulosic biomass Non-phenolic mediators 

References

  1. Ademakinwa AN, Agboola FK (2016) Biochemical characterization and kinetic studies on a purified yellow laccase from newly isolated Aureobasidium pullulans NAC8 obtained from soil containing decayed plant matter. J Genet Eng Biotechnol 14(1):143–151CrossRefPubMedPubMedCentralGoogle Scholar
  2. Afreen S, Anwer R, Singh RK et al (2018) Extracellular laccase production and its optimization from Arthrospira maxima catalyzed decolorization of synthetic dyes. Saudi J Biol Sci 25:1446–1453CrossRefPubMedGoogle Scholar
  3. Agarwal UP, Ralph SA, Reiner RS et al (2018) Production of high lignin-containing and lignin-free cellulose nanocrystals from wood. Cellulose 25:5791–5805CrossRefGoogle Scholar
  4. Andreu G, Vidal T (2011) Effects of laccase-natural mediator systems on kenaf pulp. Bioresour Technol 102(10):5932–5937CrossRefPubMedGoogle Scholar
  5. Archibald FS, Bourbonnais R, Jurasek L et al (1997) Kraft pulp bleaching and delignification by Trametes versicolor. J Biotechnol 53:215–236CrossRefGoogle Scholar
  6. Avanthi A, Banerjee R (2016) A strategic laccase mediated lignin degradation of lignocellulosic feedstocks for ethanol production. Ind Crop Prod 92:174–185CrossRefGoogle Scholar
  7. Balakshin MY, Capanema EA, Chang HM (2009) Recent advances in the isolation and analysis of lignins and lignin-carbohydrate complexes. In: Hu TQ (ed) Characterization of lignocellulosic materials. Blackwell Publishing Ltd, Oxford, pp 148–170Google Scholar
  8. Baldrian P (2006) Fungal laccases-occurrence and properties. FEMS Microbiol Rev 30:215–242CrossRefPubMedGoogle Scholar
  9. Barreca AM, Sjögren B, Fabbrini M, Gentili P (2004) Catalytic efficiency of some mediators in laccase-catalyzed alcohol oxidation. Biocat Biotransform 22(2):105–112CrossRefGoogle Scholar
  10. Bertrand B, Martínez-Morales F, Trejo-Hernandez MR (2013) Fungal laccases: induction and production. Rev Mex Ing Quim 12:473–488Google Scholar
  11. Bettin F, Montanari Q, Calloni R et al (2009) Production of laccases in submerged process by Pleurotus sajor-caju PS-2001 in relation to carbon and organic nitrogen sources, antifoams and Tween 80. J Ind Microbiol Biotechnol 36(1):1–9Google Scholar
  12. Bibi I, Bhatti HN, Asgher M (2011) Comparative study of natural and synthetic phenolic compounds as efficient laccase mediators for the transformation of cationic dye. Biochem Eng J 56:225–231CrossRefGoogle Scholar
  13. Bilal M, Asgher M, Parra-Saldivar R et al (2017) Immobilized ligninolytic enzymes: an innovative and environmental responsive technology to tackle dye-based industrial pollutants—a review. Sci Total Environ 576:646–659CrossRefPubMedGoogle Scholar
  14. Bourbonnais R, Paice M (1990) Oxidation of non-phenolic substrates: an expanded role for laccase in lignin biodegradation. FEBS Lett 207:99–102CrossRefGoogle Scholar
  15. Bourbonnais R, Paice MG, Reid ID et al (1995) Lignin oxidation by laccase isozymes from Trametes versicolor and role of the mediator 2,2′-azinobis(3 ethylbenzthiazoline-6-sulfonate) in kraft lignin depolymerization. Appl Environ Microbiol 61:1876–1880PubMedPubMedCentralGoogle Scholar
  16. Bourbonnais R, Paice MG, Freiermuth B (1997) Reactivities of various mediators and laccases with kraft pulp and lignin model compounds. Appl Environ Microbiol 63(12):4627–4632PubMedPubMedCentralGoogle Scholar
  17. Brijwani K, Rigdon A, Vadlani PV (2010) Fungal laccase: production function and applications in food processing. Enzyme Res 10:149–748Google Scholar
  18. Call HP, Mücke I (1997) History, overview and applications of mediated lignolytic systems, specially laccase-mediator-system (Lignozyme®-process). J Biotechnol 53:163–202CrossRefGoogle Scholar
  19. Camarero S, Galletti GC, Martínez AT (1994) Preferential degradation of phenolic lignin units by two white rot fungi. Appl Environ Microbiol 60:4509–4516PubMedPubMedCentralGoogle Scholar
  20. Cañas AI, Camarero S (2010) Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 28:694–705CrossRefPubMedGoogle Scholar
  21. Cardoso WS, Queiroz PV, Tavares GP et al (2018) Multi-enzyme complex of white rot fungi in saccharification of lignocellulosic material. Braz J Microbiol 49:879–884CrossRefPubMedPubMedCentralGoogle Scholar
  22. Couto SR (2018) Solid-state fermentation for laccases production and their applications. In: Current developments in biotechnology and bioengineering. Elsevier, pp 211–234Google Scholar
  23. Couto SR, Toca-Herrera JL (2007) Laccase production at reactor scale by filamentous fungi. Biotechnol Adv 25:558–569CrossRefPubMedGoogle Scholar
  24. Daroch M, Houghton CA, Moore JK et al (2014) Glycosylated yellow laccases of the basidiomycete Stropharia aeruginosa. Enzym Microb Technol 58(59):1–7CrossRefGoogle Scholar
  25. Dong JL, Zhang YW, Zhang RH et al (2005) Influence of culture conditions on laccase production and isozyme patterns in the white-rot fungus Trametes gallica. J Basic Microbiol 45:190–198CrossRefPubMedGoogle Scholar
  26. dos Santos AC, Ximenes E, Kim Y, Ladisch MR (2019) Lignin–enzyme interactions in the hydrolysis of lignocellulosic biomass. Trends Biotechnol 37(5):518–531.  https://doi.org/10.1016/j.tibtech.2018.10.010CrossRefPubMedGoogle Scholar
  27. Elisashvili V, Kachlishvili E, Asatiani D (2018) Efficient production of lignin-modifying enzymes and phenolics removal in submerged fermentation of olive mill by-products by white-rot basidiomycetes. Int Biodeterior Biodegrad 134:39–47CrossRefGoogle Scholar
  28. Enguita FJ (2011) Structural biology of fungal multicopper oxidases. In: Leitao AL (ed) Mycofactories. Bentham Science Publishers, Emirate of Sharjah, pp 57–72Google Scholar
  29. Fabbrini M, Galli C, Gentili P (2002) Comparing the catalytic efficiency of some mediators of laccase. J Mol Catal B Enzym 16:231–240CrossRefGoogle Scholar
  30. Faravelli T, Frassoldati A, Migliavacca G (2010) Detailed kinetic modeling of the thermal degradation of lignins. Biomass Bioenergy 34(3):290–301CrossRefGoogle Scholar
  31. Galbe M, Zacchi G (2007) Pretreatment of lignocellulosic materials for efficient bioethanol production. Adv Biochem Eng Biotechnol 108:41–65PubMedGoogle Scholar
  32. Gosz K, Kosmela P, Hejna A et al (2018) Biopolyols obtained via microwave-assisted liquefaction of lignin: structure, rheological, physical and thermal properties. Wood Sci Technol 52:599–617CrossRefGoogle Scholar
  33. Hatakka A (1994) Lignin-modifying enzymes from selected white-rot fungi: production and role in lignin degradation. FEMS Microbiol Rev 13:125–135CrossRefGoogle Scholar
  34. Hatakka A (2005) Biodegradation of lignin. In: Alexander S (ed) Biopolymers online. Wiley-VCH Verlag GmbH & Co. KGaA, WeinheimGoogle Scholar
  35. Hilgers R, Vincken JP, Gruppen H (2018) Laccase/mediator systems: their reactivity toward phenolic lignin structures. ACS Sustain Chem Eng 6:2037–2046CrossRefPubMedPubMedCentralGoogle Scholar
  36. Jaiswal N, Pandey VP, Dwivedi UN (2015) Immobilization of papaya laccase in chitosan led to improved multipronged stability and dye discoloration. Int J Biol Macromol 8:288–295Google Scholar
  37. Kannaiyan R, Mahinpey N, Mani T et al (2012) Enhancement of Dichomitus squalens tolerance to copper and copper-associated laccase activity by carbon and nitrogen sources. Biochem Eng J 67:140–147Google Scholar
  38. Khlifi-Slama R, Mechichi T, Sayadi S et al (2012) Effect of natural mediators on the stability of Trametes trogii laccase during the decolourization of textile wastewaters. J Microbiol 50:226–234CrossRefPubMedGoogle Scholar
  39. Kiiskinen L-L, Palonen H, Linder M, Viikari L, Kruus K (2004) Laccase from Melanocarpus albomyces binds effectively to cellulose. FEBS Lett 576:251–255CrossRefPubMedGoogle Scholar
  40. Knezevic A, Milovanović I, Stajić M et al (2013) Lignin degradation by selected fungal species. Bioresour Technol 138:117–123CrossRefPubMedGoogle Scholar
  41. Kolomytseva M, Myasoedova N, Samoilova A et al (2017) Rapid identification of fungal laccases/oxidases with different pH-optimum. Process Biochem 62:174–183CrossRefGoogle Scholar
  42. Kumar SVS, Phale PS, Durani S (2003) Combined sequence and structure analysis of the fungal laccase family. Biotechnol Bioeng 83:386–394CrossRefPubMedGoogle Scholar
  43. Li K, Xu F, Eriksson KE (1999) Comparison of fungal laccases and redox mediators in oxidation of a nonphenolic lignin model compound. Appl Environ Microbiol 65:2654–2660PubMedPubMedCentralGoogle Scholar
  44. Mainka H, Täger O, Körner E et al (2015) Lignin—an alternative precursor for sustainable and cost-effective automotive carbon fiber. J Mater Res Technol 4:283–296CrossRefGoogle Scholar
  45. Matera I, Gullotto A, Tilli S et al (2008) Crystal structure of the blue multicopper oxidase from the white-rot fungus Trametes trogii complexed with p-toluate. Inorg Chim Acta 361:4129–4137CrossRefGoogle Scholar
  46. Mikiashvili N, Wasser SP, Nevo E (2006) Effects of carbon and nitrogen sources on Pleurotus ostreatus ligninolytic enzyme activity. World J Microbiol Biotechnol 22:999–1002CrossRefGoogle Scholar
  47. Morozova OV, Shumakovich GP, Gorbacheva MA et al (2007) “Blue” laccases. J Biochem 72(10):1136–1150Google Scholar
  48. Mot AC, Silaghi-Dumitrescu R (2012) Laccases: complex architectures for one-electron oxidations. Biochemistry (Mosc) 77(12):1395–1407CrossRefGoogle Scholar
  49. Moya R, Saastamoinen P, Hernández M et al (2011) Reactivity of bacterial and fungal laccases with lignin under alkaline conditions. Bioresour Technol 102(21):10006–10012CrossRefPubMedGoogle Scholar
  50. Munk L, Punt AM, Kabel MA (2018) Laccase catalyzed grafting of-N-OH type mediators to lignin via radical-radical coupling. RSC Adv 7(6):3358–3368CrossRefGoogle Scholar
  51. Murciano Martínez P, Punt AM, Kabel MA et al (2016) Deconstruction of lignin linked p-coumarates, ferulates and xylan by NaOH enhances the enzymatic conversion of glucan. Bioresour Technol 216:44–51CrossRefPubMedGoogle Scholar
  52. Musatti A, Ficara E, Mapelli C (2017) Use of solid digestate for lignocellulolytic enzymes production through submerged fungal fermentation. J Environ Manag 199:1–6CrossRefGoogle Scholar
  53. Ning YJ, Wang SS, Chen QJ, Ling ZR, Wang SN, Wang WP, Zhang GQ, Zhu MJ (2016) An extracellular yellow laccase with potent dye decolorizing ability from the fungus Leucoagaricus naucinus LAC-04. Int J Biol Macromol 93:837–842CrossRefPubMedGoogle Scholar
  54. Palmieri G, Giardina P, Bianco C et al (1997) A novel white laccase from Pleurotus ostreatus. J Biol Chem 272:31301–31307CrossRefPubMedGoogle Scholar
  55. Piscitelli A, Pezzella C, Giardina P (2010) Heterologous laccase production and its role in industrial applications. Bioeng Bugs 1:252–262CrossRefPubMedPubMedCentralGoogle Scholar
  56. Plácido J, Capareda S (2015) Ligninolytic enzymes: a biotechnological alternative for bioethanol production. Bioresour Bioprocess 2:23CrossRefGoogle Scholar
  57. Pointing SB, Jones EBG, Vrijmoed LLP (2000) Optimization of laccase production by Pycnoporus sanguineus in submerged liquid culture. Mycologia 92(1):139–144CrossRefGoogle Scholar
  58. Poppius-Levlin K, Whang W, Tamminen T et al (1999) Effects of laccase/HBT treatment on pulp and lignin structures. J Pulp Pap Sci 25:90–94Google Scholar
  59. Potthast A, Koch H, Fischer K (1997) The laccase-mediator system—reaction with model compounds and pulp. In: Preprints 9th international symposium wood pulp (Montreal, Canada), S. F1-4–F1-8. Chem Tech Section F2-1–F2-4Google Scholar
  60. Pozdnyakova N, Rodakiewicz-Nowak J, Turkovskaya O (2004) Catalytic properties of yellow laccase from Pleurotus ostreatus D1. J Mol Catal B Enzym 30:19–24CrossRefGoogle Scholar
  61. Pozdnyakova NN, Rodakiewicz-Nowak J, Turkovskaya OV, Haber J (2006a) Oxidative degradation of polyaromatic hydrocarbons and their derivatives catalyzed directly by the yellow laccase from Pleurotus ostreatus D1. J Mol Catal B Enzym 41:8–15CrossRefGoogle Scholar
  62. Pozdnyakova NN, Turkovskaya OV, Yudina EN (2006b) Yellow laccase from the fungus Pleurotus ostreatus D1: purification and characterization. Appl Biochem Microbiol 42(1):56–61Google Scholar
  63. Prasad R (2018) Mycoremediation and environmental sustainability. Springer International Publishing, ChamCrossRefGoogle Scholar
  64. Reddy GV, Ravindra BP, Komaraiah P (2003) Utilization of banana waste for the production of lignolytic and cellulolytic enzymes by solid substrate fermentation using two Pleurotus species (P. ostreatus and P. sajor-caju). Process Biochem 38:1457–1462CrossRefGoogle Scholar
  65. Rivera-Hoyos CM, Morales-Alverez ED, Poutou-Pinales RA et al (2013) Fungal laccases. Fungal Biol Rev 27(3–4):67–82CrossRefGoogle Scholar
  66. Robinson T, Chandran B, Nigam P (2001) Studies on the production of enzymes by white-rot fungi for the decolourisation of textile dyes. Enzyme Microb Technol 29:575–579CrossRefGoogle Scholar
  67. Rodriguez 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):612–616Google Scholar
  68. Rudakiya DM, Gupte A (2017) Degradation of hardwoods by treatment of white rot fungi and its pyrolysis kinetics studies. Int Biodeter Biodegr 120:21–35CrossRefGoogle Scholar
  69. Ruiz-Dueñas FJ, Martínez ÁT (2009) Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microb Biotechnol 2:164–177CrossRefPubMedPubMedCentralGoogle Scholar
  70. Rytioja J, Hildén K, Mäkinen S et al (2014) Saccharification of lignocelluloses by Carbohydrate Active Enzymes of the white rot fungus Dichomitus squalens. PLoS One 10(12):e0145166CrossRefGoogle Scholar
  71. Saito Y, Tsuchida H, Matsumoto T et al (2018) Screening of fungi for decomposition of lignin-derived products from Japanese cedar. J Biosci Bioeng 126:573–579CrossRefPubMedGoogle Scholar
  72. Schlosser D, Hofer C (2002) Laccase-catalyzed oxidation of Mn2+ in the presence of natural Mn3+ chelators as a novel source of extracellular H2O2 production and its impact on manganese peroxidase. Appl Environ Microbiol 68(7):3514–3521CrossRefPubMedPubMedCentralGoogle Scholar
  73. Shankar S, Shikha (2011) Fungal laccases: production and biotechnological applications in pulp and paper industry. In: Jain PK, Gupta VK, Bajpai V (eds) Recent advances in environmental biotechnology. Dudweller Landstr, Saarbrücken, pp 73–111Google Scholar
  74. Shankar S, Shikha (2012) Laccase production and enzymatic modification of lignin by a novel Peniophora sp. Appl Biochem Biotechnol 166:1082–1094CrossRefPubMedGoogle Scholar
  75. Shankar S, Shikha (2015) Effects of metal ions and redox mediator system on decolorization of synthetic dyes by crude laccase from a novel white rot fungus Peniophora sp. (NFCCI-2131). Appl Biochem Biotechnol 175(1):635–647CrossRefPubMedGoogle Scholar
  76. Sharma P, Goel R, Capalash N (2007) Bacterial laccases. World J Microbiol Biotechnol 23:823–832CrossRefGoogle Scholar
  77. Sigoillot JC, Berrin JG, Bey M et al (2012) Fungal strategies for lignin degradation. In: Jouanin L, Lapierre C (eds) Lignins: biosynthesis, biodegradation and bioengineering, vol 61. Academic, Elsevier, London, pp 263–308CrossRefGoogle Scholar
  78. Singh H (2006) Mycoremediation: fungal bioremediation, 1st edn. Wiley-Interscience. ISBN-13: 978-0471755012Google Scholar
  79. Siqueira G, Várnai A, Ferraz A et al (2012) Enhancement of cellulose hydrolysis in sugarcane bagasse by the selective removal of lignin with sodium chlorite. Appl Energy 102:399–402CrossRefGoogle Scholar
  80. Surwase SV, Patil SA, Srinivas S et al (2016) Interaction of small molecules with fungal laccase: a surface plasmon resonance based study. Enzym Microb Technol 82:110–114CrossRefGoogle Scholar
  81. Thiruchelvam AT, Ramsay JA (2007) Growth and laccase production kinetics of Trametes versicolor in a stirred tank reactor. Appl Microbiol Biotechnol 74:547–554CrossRefPubMedGoogle Scholar
  82. Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140:19–26CrossRefGoogle Scholar
  83. Wang SN, Chen QJ, Zhu MJ et al (2018) An extracellular yellow laccase from white rot fungus Trametes sp. F1635 and its mediator systems for dye decolorization. Biochimie 148:46–54CrossRefPubMedGoogle Scholar
  84. Wu F, Ozaki H, Terashima Y et al (1996) Activities of ligninolytic enzymes of the white rot fungus, and its recalcitrant substance degradability. Water Sci Technol 34:69–78CrossRefGoogle Scholar
  85. Xavier AMRB, Evtuguin DV, Ferreira RMP et al (2001) Laccase production for lignin oxidative activity. In: Proceedings of the 8th international conference on biotechnology in the pulp and paper industry, 4–8 June, HelsinkiGoogle Scholar
  86. Xu F (1997) Effects of redox potential and hydroxide inhibition on the pH activity profile of fungal laccases. J Biol Chem 272(2):924–928CrossRefPubMedGoogle Scholar
  87. Yaohua G, Ping X, Feng J et al (2019) Co-immobilization of laccase and ABTS onto novel dual-functionalized cellulose beads for highly improved biodegradation of indole. J Hazard Mater 365:118–124CrossRefPubMedGoogle Scholar
  88. Young D, Dollhofer V, Callaghan TM et al (2018) Isolation, identification and characterization of lignocellulolytic aerobic and anaerobic fungi in one- and two-phase biogas plants. Bioresour Technol 268:470–479CrossRefPubMedGoogle Scholar
  89. Zhao D, Zhang X, Cui DZ (2012) Characterisation of a novel white laccase from the deuteromycete fungus Myrothecium verrucaria NF-05 and its decolourisation of dyes. PLoS One 7:e38817CrossRefPubMedPubMedCentralGoogle Scholar
  90. Zhu G, Ouyang X, Jiang L et al (2016) Effect of functional groups on hydrogenolysis of lignin model compounds. Fuel Process Technol 154:132–138CrossRefGoogle Scholar
  91. Zille A, Tzanov T, Gübitz GM (2003) Immobilized laccase for decolourization of reactive black 5 dyeing effluent. Biotechnol Lett 25:1473–1477CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Shiv Shankar
    • 1
  • Shailja Singh
    • 2
  • Shikha
    • 2
  • Anuradha Mishra
    • 1
  • Siya Ram
    • 3
  1. 1.Department of Environmental ScienceSchool of Vocational Studies and Applied Sciences, Gautam Budhha University (A State University)Greater NoidaIndia
  2. 2.Department of Environmental ScienceSchool for Environmental Sciences, Babasaheb Bhimrao Ambedkar University (A Central University)LucknowIndia
  3. 3.Department of BiotechnologySchool of Biotechnology, Gautam Budhha University (A State University)Greater NoidaIndia

Personalised recommendations