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Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Review Article

Mechanisms of Lignin-Degrading Enzymes

Author(s): Jianlong Xiao, Sitong Zhang* and Guang Chen*

Volume 27, Issue 7, 2020

Page: [574 - 581] Pages: 8

DOI: 10.2174/0929866527666191223141756

Price: $65

Abstract

Lignin is abundant in nature. It is a potentially valuable bioresource, but, because of its complex structure, it is difficult to degrade. However, enzymatic degradation of lignin is effective. Major lignin-degrading enzymes include laccases, lignin peroxidases, and manganese peroxidases. In this paper, the mechanisms of degradation of lignin by these three enzymes is reviewed, and synergy between them is discussed.

Keywords: Lignin, laccase, lignin peroxidase, manganese peroxidase, degradation mechanism, bioresource.

Graphical Abstract

[1]
Jönsson, L.J.; Martín, C. Pretreatment of lignocellulose: Formation of inhibitory by-products and strategies for minimizing their effects. Bioresour. Technol., 2016, 199, 103-112.
[http://dx.doi.org/10.1016/j.biortech.2015.10.009] [PMID: 26482946]
[2]
Li, H.; Dai, M.; Dai, S.; Dong, X. Current status and environment impact of direct straw return in China’s cropland - A review. Ecotoxicol. Environ. Saf., 2018, 159, 293-300.
[http://dx.doi.org/10.1016/j.ecoenv.2018.05.014] [PMID: 29763811]
[3]
Yan, X.; Ohara, T.; Akimoto, H. Bottom-up estimate of biomass burning in mainland China. Atmos. Environ., 2006, 40(27), 5262-5273.
[http://dx.doi.org/10.1016/j.atmosenv.2006.04.040]
[4]
Liu, H.; Ou, X.; Yuan, J. Experience of producing natural gas from corn straw in China. Resour. Conserv. Recycling, 2018, 135, 216-224.
[http://dx.doi.org/10.1016/j.resconrec.2017.10.005]
[5]
Chen, Y.A.; Zhou, Y.; Qin, Y.; Liu, D.; Zhao, X. Evaluation of the action of Tween 20 non-ionic surfactant during enzymatic hydrolysis of lignocellulose: Pretreatment, hydrolysis conditions and lignin structure. Bioresour. Technol., 2018, 269, 329-338.
[http://dx.doi.org/10.1016/j.biortech.2018.08.119] [PMID: 30195225]
[6]
Pardo, I.; Vicente, A.I.; Mate, D.M.; Alcalde, M.; Camarero, S. Development of chimeric laccases by directed evolution. biotechnol. bioeng., 2012, 109(12), 2978-2986.
[http://dx.doi.org/10.1002/bit.24588] [PMID: 22729887]
[7]
Khan, M.U.; Ahring, B.K. Lignin degradation under anaerobic digestion: Influence of lignin modifications -A review. Biomass Bioenergy, 2019, 128, 105325.
[http://dx.doi.org/10.1016/j.biombioe.2019.105325]
[8]
Asina, F.; Brzonova, I.; Voeller, K.; Kozliak, E.; Kubátová, A.; Yao, B.; Ji, Y. Biodegradation of lignin by fungi, bacteria and laccases. Bioresour. Technol., 2016, 220, 414-424.
[http://dx.doi.org/10.1016/j.biortech.2016.08.016] [PMID: 27598570]
[9]
Brodeur, G.; Yau, E.; Badal, K.; Collier, J.; Ramachandran, K.B.; Ramakrishnan, S. Chemical and physicochemical pretreatment of lignocellulosic biomass: a review. Enzyme Res., 2011, 2011, 787532.
[http://dx.doi.org/10.4061/2011/787532] [PMID: 21687609]
[10]
Dinis, M.J.; Bezerra, R.M.F.; Nunes, F.; Dias, A.A.; Guedes, C.V.; Ferreira, L.M.; Cone, J.W.; Marques, G.S.; Barros, A.R.; Rodrigues, M.A. Modification of wheat straw lignin by solid state fermentation with white-rot fungi. Bioresour. Technol., 2009, 100(20), 4829-4835.
[http://dx.doi.org/10.1016/j.biortech.2009.04.036] [PMID: 19450975]
[11]
Mikiashvili, N.; Wasser, S.P.; Nevo, E. Effects of carbon and nitrogen sources on Pleurotus ostreatus ligninolytic enzyme activity. World J. Microbiol. Biotechnol., 2006, 22(9), 999-1002.
[http://dx.doi.org/10.1007/s11274-006-9132-6]
[12]
Perez, J; Munoz-Dorado, J; de la Rubia, T.; Martínez, J. Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview. Int. Microbiol., 2002, 5(2), 53-63.
[http://dx.doi.org/10.1007/s10123-002-0062-3]
[13]
Iandolo, D.; Amore, A.; Birolo, L.; Leo, G.; Olivieri, G.; Faraco, V. Fungal solid state fermentation on agro-industrial wastes for acid wastewater decolorization in a continuous flow packed-bed bioreactor. Bioresour. Technol., 2011, 102(16), 7603-7607.
[http://dx.doi.org/10.1016/j.biortech.2011.05.029] [PMID: 21652205]
[14]
Hoegger, P.J.; Kilaru, S.; James, T.Y.; Thacker, J.R.; Kües, U. Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J., 2006, 273(10), 2308-2326.
[http://dx.doi.org/10.1111/j.1742-4658.2006.05247.x] [PMID: 16650005]
[15]
Alexandre, G.; Zhulin, I.B. Laccases are widespread in bacteria. Trends Biotechnol., 2000, 18(2), 41-42.
[http://dx.doi.org/10.1016/S0167-7799(99)01406-7] [PMID: 10652504]
[16]
Sidjanski, S.; Mathews, G.V.; Vanderberg, J.P. Electrophoretic separation and identification of phenoloxidases in hemolymph and midgut of adult Anopheles stephensi mosquitoes. J. Parasitol., 1997, 83(4), 686-691.
[http://dx.doi.org/10.2307/3284247] [PMID: 9267412]
[17]
Ghosh, B.; Saha, R.; Bhattacharya, D. Laccase and its source of sustainability in an enzymatic biofuel cell. Bioresour. Technol. Reports, 2019, 6, 268-278.
[http://dx.doi.org/10.1016/j.biteb.2019.03.013]
[18]
Rivera-Hoyos, C.M.; Morales-Álvarez, E.D.; Poutou-Piñales, R.A. Fungal laccases. Fungal Biol. Rev., 2013, 27(3-4), 67-82.
[http://dx.doi.org/10.1016/j.fbr.2013.07.001]
[19]
Rekadwad, B.; Khobragade, C. Fungi Imperfecti Laccase: Biotechnological Potential and Perspectives. in: Microbial Applications; Springer International Publishing: Cham, 2017, Vol. 2, pp. 203-212.
[http://dx.doi.org/10.1007/978-3-319-52669-0_11]
[20]
Ibrahim, V.; Mendoza, L.; Mamo, G. Blue laccase from Galerina sp.: Properties and potential for Kraft lignin demethylation. Process Biochem., 2011, 46(1), 379-384.
[http://dx.doi.org/10.1016/j.procbio.2010.07.013]
[21]
Baldrian, P. Fungal laccases - occurrence and properties. FEMS Microbiol. Rev., 2006, 30(2), 215-242.
[http://dx.doi.org/10.1111/j.1574-4976.2005.00010.x] [PMID: 16472305]
[22]
Su, J.; Fu, J.; Wang, Q.; Silva, C.; Cavaco-Paulo, A. Laccase: a green catalyst for the biosynthesis of poly-phenols. Crit. Rev. Biotechnol., 2018, 38(2), 294-307.
[http://dx.doi.org/10.1080/07388551.2017.1354353] [PMID: 28738694]
[23]
Brissos, V.; Pereira, L.; Munteanu, F.D.; Cavaco-Paulo, A.; Martins, L.O. Expression system of CotA-laccase for directed evolution and high-throughput screenings for the oxidation of highredox potential dyes. Biotechnol. J., 2009, 4(4), 558-563.
[http://dx.doi.org/10.1002/biot.200800248] [PMID: 19156728]
[24]
Gellissen, G.; Hollenberg, C.P. Application of yeasts in gene expression studies: a comparison of Saccharomyces cerevisiae, Hansenula polymorpha and Kluyveromyces lactis -- a review. Gene, 1997, 190(1), 87-97.
[http://dx.doi.org/10.1016/S0378-1119(97)00020-6] [PMID: 9185853]
[25]
Hong, Y.; Xiao, Y.; Zhou, H.; Fang, W.; Zhang, M.; Wang, J.; Wu, L.; Yu, Z. Expression of a laccase cDNA from Trametes sp. AH28-2 in Pichia pastoris and mutagenesis of transformants by nitrogen ion implantation. FEMS Microbiol. Lett., 2006, 258(1), 96-101.
[http://dx.doi.org/10.1111/j.1574-6968.2006.00209.x] [PMID: 16630262]
[26]
Thanh Mai Pham, L.; Eom, M.H.; Kim, Y.H. Inactivating effect of phenolic unit structures on the biodegradation of lignin by lignin peroxidase from Phanerochaete chrysosporium. Enzyme Microb. Technol., 2014, 61-62, 48-54.
[http://dx.doi.org/10.1016/j.enzmictec.2014.04.013] [PMID: 24910336]
[27]
Pham, T.M.; Kim, Y.H. Accelerated degradation of lignin by lignin peroxidase isozyme H8 (LiPH8) from Phanerochaete chrysosporium with engineered 4-O-methyltransferase from Clarkia breweri. Enzyme Microb. Technol., 2014, 66, 74-79.
[http://dx.doi.org/10.1016/j.enzmictec.2014.08.011] [PMID: 25248703]
[28]
Falade, A.O.; Eyisi, O.A.L.; Mabinya, L.V.; Nwodo, U.U.; Okoh, A.I. Peroxidase production and ligninolytic potentials of fresh water bacteria Raoultella ornithinolytica and Ensifer adhaerens. . Biotechnol. Rep. (Amst.), 2017, 16, 12-17.
[http://dx.doi.org/10.1016/j.btre.2017.10.001] [PMID: 29062721]
[29]
Choinowski, T.; Blodig, W.; Winterhalter, K.H.; Piontek, K. The crystal structure of lignin peroxidase at 1.70 A resolution reveals a hydroxy group on the cbeta of tryptophan 171: a novel radical site formed during the redox cycle. J. Mol. Biol., 1999, 286(3), 809-827.
[http://dx.doi.org/10.1006/jmbi.1998.2507] [PMID: 10024453]
[30]
Camarero, S.; Sarkar, S.; Ruiz-Dueñas, F.J.; Martínez, M.J.; Martínez, A.T. Description of a versatile peroxidase involved in the natural degradation of lignin that has both manganese peroxidase and lignin peroxidase substrate interaction sites. J. Biol. Chem., 1999, 274(15), 10324-10330.
[http://dx.doi.org/10.1074/jbc.274.15.10324] [PMID: 10187820]
[31]
Cai, D.; Tien, M. Lignin-degrading peroxidases of Phanerochaete chrysosporium. J. Biotechnol., 1993, 30(1), 79-90.
[http://dx.doi.org/10.1016/0168-1656(93)90029-M] [PMID: 7763834]
[32]
Kersten, P.J. Glyoxal oxidase of Phanerochaete chrysosporium: its characterization and activation by lignin peroxidase. Proc. Natl. Acad. Sci. USA, 1990, 87(8), 2936-2940.
[http://dx.doi.org/10.1073/pnas.87.8.2936] [PMID: 11607073]
[33]
Ma, R.; Guo, M.; Zhang, X. Recent advances in oxidative valorization of lignin. Catal. Today, 2018, 302, 50-60.
[http://dx.doi.org/10.1016/j.cattod.2017.05.101]
[34]
Hammel, K.E.; Jensen, K.A., Jr.; Mozuch, M.D.; Landucci, L.L.; Tien, M.; Pease, E.A. Ligninolysis by a purified lignin peroxidase. J. Biol. Chem., 1993, 268(17), 12274-12281.
[PMID: 8509364]
[35]
Huang, S.; Huang, D.; Wu, Q.; Hou, M.; Tang, X.; Zhou, J. The effects of environmental C/N on the activities of lignin-degrading enzymes produced by Phanerochaete chrysosporium. Pedosphere, 2017. Epub ahead of print
[http://dx.doi.org/10.1016/S1002-0160(17)60391-6]
[36]
Johnson, T.M.; Li, J.K. Heterologous expression and characterization of an active lignin peroxidase from Phanerochaete chrysosporium using recombinant baculovirus. Arch. Biochem. Biophys., 1991, 291(2), 371-378.
[http://dx.doi.org/10.1016/0003-9861(91)90148-C] [PMID: 1952950]
[37]
Johnson, T.M.; Pease, E.A.; Li, J.K.; Tien, M. Production and characterization of recombinant lignin peroxidase isozyme H2 from Phanerochaete chrysosporium using recombinant baculovirus. Arch. Biochem. Biophys., 1992, 296(2), 660-666.
[http://dx.doi.org/10.1016/0003-9861(92)90624-6] [PMID: 1632652]
[38]
Wang, W.; Wen, X. Expression of lignin peroxidase H2 from Phanerochaete chrysosporium by multi-copy recombinant Pichia strain. J. Environ. Sci. (China), 2009, 21(2), 218-222.
[http://dx.doi.org/10.1016/S1001-0742(08)62254-8] [PMID: 19402425]
[39]
Bermek, H.; Yazıcı, H.; Öztürk, H. Purification and characterization of manganese peroxidase from wood-degrading fungus Trichophyton rubrum LSK-27. Enzyme Microb. Technol., 2004, 35(1), 87-92.
[http://dx.doi.org/10.1016/j.enzmictec.2004.04.004]
[40]
Orth, A.B.; Royse, D.J.; Tien, M. Ubiquity of lignin-degrading peroxidases among various wood-degrading fungi. Appl. Environ. Microbiol., 1993, 59(12), 4017-4023.
[PMID: 8285705]
[41]
Ninomiya, R.; Zhu, B.; Kojima, T.; Iwasaki, Y.; Nakano, H. Role of disulfide bond isomerase DsbC, calcium ions, and hemin in cellfree protein synthesis of active manganese peroxidase isolated from Phanerochaete chrysosporium. J. Biosci. Bioeng., 2014, 117(5), 652-657.
[http://dx.doi.org/10.1016/j.jbiosc.2013.11.003] [PMID: 24332478]
[42]
Chen, W.; Zheng, L.; Jia, R. Cloning and expression of a new manganese peroxidase from Irpex lacteus F17 and its application in decolorization of reactive black 5. Process Biochem., 2015, 50(11), 1748-1759.
[http://dx.doi.org/10.1016/j.procbio.2015.07.009]
[43]
Sundaramoorthy, M.; Gold, M.H.; Poulos, T.L. Ultrahigh (0.93A) resolution structure of manganese peroxidase from Phanerochaete chrysosporium: implications for the catalytic mechanism. J. Inorg. Biochem., 2010, 104(6), 683-690.
[http://dx.doi.org/10.1016/j.jinorgbio.2010.02.011] [PMID: 20356630]
[44]
Sundaramoorthy, M.; Kishi, K.; Gold, M.H.; Poulos, T.L. The crystal structure of manganese peroxidase from Phanerochaete chrysosporium at 2.06-A resolution. J. Biol. Chem., 1994, 269(52), 32759-32767.
[PMID: 7806497]
[45]
Kishi, K.; Wariishi, H.; Marquez, L.; Dunford, H.B.; Gold, M.H. Mechanism of manganese peroxidase compound II reduction. effect of organic acid chelators and ph. biochemistry, 1994, 33(29), 8694-8701.
[http://dx.doi.org/10.1021/bi00195a010] [PMID: 8038159]
[46]
Agarwal, A.; Rana, M.; Park, J. Advancement in technologies for the depolymerization of lignin. Fuel Process. Technol., 2018, 181, 115-132.
[http://dx.doi.org/10.1016/j.fuproc.2018.09.017]
[47]
Whitwam, R.; Tien, M. Heterologous expression and reconstitution of fungal Mn peroxidase., arch. biochem. biophys. 1996, 333(2), 439-446.
[http://dx.doi.org/10.1006/abbi.1996.0413] [PMID: 8809085]
[48]
Stewart, P.; Whitwam, R.E.; Kersten, P.J.; Cullen, D.; Tien, M. Efficient expression of a Phanerochaete chrysosporium manganese peroxidase gene in Aspergillus oryzae. Appl. Environ. Microbiol., 1996, 62(3), 860-864.
[49]
Janusz, G.; Kucharzyk, K.H.; Pawlik, A.; Staszczak, M.; Paszczynski, A.J. fungal laccase, manganese peroxidase and lignin peroxidase: gene expression and regulation. enzyme microb. technol., 2013, 52(1), 1-12.
[http://dx.doi.org/10.1016/j.enzmictec.2012.10.003] [PMID: 23199732]
[50]
Bugg, T.D.; Ahmad, M.; Hardiman, E.M.; Rahmanpour, R. Pathways for degradation of lignin in bacteria and fungi. Nat. Prod. Rep., 2011, 28(12), 1883-1896.
[http://dx.doi.org/10.1039/c1np00042j] [PMID: 21918777]
[51]
Knežević, A.; Milovanović, I.; Stajić, M.; Lončar, N.; Brčeski, I.; Vukojević, J.; Cilerdžić, J. Lignin degradation by selected fungal species. Bioresour. Technol., 2013, 138, 117-123.
[http://dx.doi.org/10.1016/j.biortech.2013.03.182] [PMID: 23612169]
[52]
Abbas, A.; Koc, H.; Liu, F.; Tien, M. Fungal degradation of wood: initial proteomic analysis of extracellular proteins of Phanerochaete chrysosporium grown on oak substrate. Curr. Genet., 2005, 47(1), 49-56.
[http://dx.doi.org/10.1007/s00294-004-0550-4] [PMID: 15551134]
[53]
Leonowicz, A.; Cho, N.S.; Luterek, J.; Wilkolazka, A.; Wojtas-Wasilewska, M.; Matuszewska, A.; Hofrichter, M.; Wesenberg, D.; Rogalski, J. Fungal laccase: properties and activity on lignin. J. Basic Microbiol., 2001, 41(3-4), 185-227.
[http://dx.doi.org/10.1002/1521-4028(200107)41:3/4<185::AIDJOBM185>3.0.CO;2-T] [PMID: 11512451]
[54]
McMahon, A.M.; Doyle, E.M.; Brooks, S. Biochemical characterisation of the coexisting tyrosinase and laccase in the soil bacterium Pseudomonas putida F6. Enzyme Microb. Technol., 2007, 40(5), 1435-1441.
[http://dx.doi.org/10.1016/j.enzmictec.2006.10.020]
[55]
Hildén, L.; Johansson, G.; Pettersson, G.; Li, J.; Ljungquist, P.; Henriksson, G. Do the extracellular enzymes cellobiose dehydrogenase and manganese peroxidase form a pathway in lignin biodegradation? FEBS Lett., 2000, 477(1-2), 79-83.
[http://dx.doi.org/10.1016/S0014-5793(00)01757-9] [PMID: 10899314]
[56]
Behera, S.; Arora, R.; Nandhagopal, N. Importance of chemical pretreatment for bioconversion of lignocellulosic biomass. Renew. Sustain. Energy Rev., 2014, 36, 91-106.
[http://dx.doi.org/10.1016/j.rser.2014.04.047]

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