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Fungal Enzymatic Degradation of Cellulose

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Abstract

In nature, filamentous fungi are potent degraders of cellulose as they are able to produce a high number and broad variety of cellulases with complementary catalytic activities. These enzymes include notably classical glycoside hydrolase activities, i.e., endoglucanases, cellobiohydrolases, and β-glucosidases. Oxidative enzymes are also involved in cellulose deconstruction, such as the newly discovered lytic polysaccharide monooxygenases (LPMOs), and auxiliary nonenzymatic proteins are involved in substrate targeting and loosening. In this chapter, the actions of the enzymatic partners are described, as well as their kinetics and the interactions between cellulases and with non cellulase enzymes (i.e., synergism). Because recalcitrant cellulose is still a challenge to date, strategies to discover new efficient biocatalysts from fungal biodiversity are also presented here.

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References

  • Alfaro M, Oguiza JA, Ramírez L et al (2014) Comparative analysis of secretomes in basidiomycete fungi. J Proteomics 102:28–43

    Article  Google Scholar 

  • Åkerholm M, Salmén L (2001) Interactions between wood polymers studied by dynamic FT-IR spectroscopy. Polymer 42(3):963–969

    Article  Google Scholar 

  • Andberg M, Penttilä M, Saloheimo M (2015) Swollenin from Trichoderma reesei exhibits hydrolytic activity against cellulosic substrates with features of both endoglucanases and cellobiohydrolases. Biores Technol 181:105–113

    Article  Google Scholar 

  • Arfi Y, Chevret D, Henrissat B et al (2013) Characterization of salt-adapted secreted lignocellulolytic enzymes from the mangrove fungus Pestalotiopsis sp. Nat Commun 4:1810

    Article  Google Scholar 

  • Bansal P, Hall M, Realff MJ et al (2009) Modeling cellulase kinetics on lignocellulosic substrates. Biotechnol Adv 27(6):833–848

    Article  Google Scholar 

  • Beeson WT, Phillips CM, Cate JH et al (2012) Oxidative cleavage of cellulose by fungal copper-dependent polysaccharide monooxygenases. J Am Chem Soc 134(2):890–892

    Article  Google Scholar 

  • Benko Z, Siika-aho M, Viikari L et al (2008) Evaluation of the role of xyloglucanase in the enzymatic hydrolysis of lignocellulosic substrates. Enzyme Microb Technol 43(2):109–114

    Article  Google Scholar 

  • Bennati-Granier C, Garajova S, Champion C et al (2015) Substrate specificity and regioselectivity of fungal AA9 lytic polysaccharide monooxygenases secreted by Podospora anserina. Biotechnol Biofuels 8(1):90

    Article  Google Scholar 

  • Berrin JG, Navarro D, Couturier M et al (2012) Exploring the natural fungal biodiversity of tropical and temperate forests toward improvement of biomass conversion. Appl Environ Microbiol 78(18):6483–6490

    Article  Google Scholar 

  • Bey M, Zhou S, Poidevin L et al (2013) Cello-oligosaccharide oxidation reveals differences between two lytic polysaccharide monooxygenases (Family GH61) from Podospora anserina. Appl Environ Microbiol 79(2):488–496

    Article  Google Scholar 

  • Boraston AB, Bolam DN, Gilbert HJ et al (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781

    Article  Google Scholar 

  • Borisova AS, Isaksen T, Dimarogona M et al (2015) Structural and functional characterization of a lytic polysaccharide monooxygenase with broad substrate specificity. J Biol Chem 290(38):22955–22969

    Article  Google Scholar 

  • Chen Y, Stipanovic AJ, Winter WT et al (2007) Effect of digestion by pure cellulases on crystallinity and average chain length for bacterial and microcrystalline celluloses. Cellulose 14:283–293

    Article  Google Scholar 

  • Chen X, Ishida N, Todaka N et al (2010) Promotion of efficient Saccharification of crystalline cellulose by Aspergillus fumigatus Swo1. Appl Environ Microbiol 76(8):2556–2561

    Article  Google Scholar 

  • Cosgrove DJ (2014) Re-constructing our models of cellulose and primary cell wall assembly. Curr Opin Plant Biol 22:122–131

    Article  Google Scholar 

  • Couturier M, Haon M, Coutinho PM et al (2011) Podospora anserina hemicellulases potentiate the trichoderma reesei secretome for saccharification of lignocellulosic biomass. Appl Environ Microbiol 77(1):237–246

    Article  Google Scholar 

  • Couturier M, Navarro D, Olivé C et al (2012) Post-genomic analyses of fungal lignocellulosic biomass degradation reveal the unexpected potential of the plant pathogen Ustilago maydis. BMC Genom 13(1):57

    Article  Google Scholar 

  • Davies G, Henrissat B (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3(9):853–859

    Article  Google Scholar 

  • Dimarogona M, Topakas E, Olsson L et al (2012) Lignin boosts the cellulase performance of a GH-61 enzyme from Sporotrichum thermophile. Biores Technol 110:480–487

    Article  Google Scholar 

  • Floudas D, Binder M, Riley R et al (2012) The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719

    Article  Google Scholar 

  • Floudas D, Held BW, Riley R et al (2015) Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii. Fungal Genet Biol 76:78–92

    Article  Google Scholar 

  • Forsberg Z, Vaaje-Kolstad G, Westereng B et al (2011) Cleavage of cellulose by a CBM33 protein. Protein Sci 20(9):1479–1483

    Article  Google Scholar 

  • Gao D, Uppugundla N, Chundawat SP et al (2011) Hemicellulases and auxiliary enzymes for improved conversion of lignocellulosic biomass to monosaccharides. Biotechnol Biofuels 4(1):5

    Article  Google Scholar 

  • Gao D, Haarmeyer C, Balan V et al (2014) Lignin triggers irreversible cellulase loss during pretreated lignocellulosic biomass saccharification. Biotechnol Biofuels 7(1):175

    Article  Google Scholar 

  • Gourlay K, Hu J, Arantes V et al (2013) Swollenin aids in the amorphogenesis step during the enzymatic hydrolysis of pretreated biomass. Biores Technol 142:498–503

    Article  Google Scholar 

  • Guillén D, Sánchez S, Rodríguez-Sanoja R (2010) Carbohydrate-binding domains: multiplicity of biological roles. Appl Microbiol Biotechnol 85:1241–1249

    Article  Google Scholar 

  • Guo F, Shi W, Sun W et al (2014) Differences in the adsorption of enzymes onto lignins from diverse types of lignocellulosic biomass and the underlying mechanism. Biotechnol Biofuels 7(1):38

    Article  Google Scholar 

  • Harris PV, Welner D, McFarland KC et al (2010) Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: structure and function of a large, enigmatic family. Biochem 49(15):3305–3316

    Article  Google Scholar 

  • Hemsworth GR, Henrissat B, Davies GJ et al (2014) Discovery and characterization of a new family of lytic polysaccharide monooxygenases. Nat Chem Biol 10(2):122–126

    Article  Google Scholar 

  • Harris PV, Xu F, Kreel NE et al (2014) New enzyme insights drive advances in commercial ethanol production. Curr Opin Chem Biol 19:162–170

    Article  Google Scholar 

  • Hemsworth GR, Taylor EJ, Kim RQ et al (2013) The copper active site of CBM33 polysaccharide oxygenases. J Am Chem Soc 135(16):6069–6077

    Article  Google Scholar 

  • Henrissat B, Vegetales M, Grenoble F (1991) A classification of glycosyl hydrolases based sequence similarities amino acid. Biochem J 280:309–316

    Article  Google Scholar 

  • Hu J, Arantes V, Saddler JN (2011) The enhancement of enzymatic hydrolysis of lignocellulosic substrates by the addition of accessory enzymes such as xylanase: is it an additive or synergistic effect? Biotechnol Biofuels 4(1):36

    Article  Google Scholar 

  • Igarashi K, Uchihashi T, Koivula A et al (2011) Traffic jams reduce hydrolytic efficiency of cellulase on cellulose surface. Science 333(6047):1279–1282

    Article  Google Scholar 

  • Isaksen T, Westereng B, Aachmann FL et al (2014) A C4-oxidizing lytic polysaccharide monooxygenase cleaving both cellulose and cello-oligosaccharides. J Biol Chem 289(5):2632–2642

    Article  Google Scholar 

  • Jeng WY, Wang NC, Lin MH et al (2011) Structural and functional analysis of three β-glucosidases from bacterium Clostridium cellulovorans, fungus Trichoderma reesei and termite Neotermes koshunensis. J Struct Biol 173(1):46–56

    Article  Google Scholar 

  • Kämper J, Kahmann R, Bölker M et al (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444(7115):97–101

    Article  Google Scholar 

  • Karkehabadi S, Hansson H, Kim S et al (2008) The first structure of a glycoside hydrolase family 61 member, Cel61B from Hypocrea jecorina, at 1.6Å Resolution. J Mol Biol 383(1):144–154

    Article  Google Scholar 

  • Karkehabadi S, Helmich KE, Kaper T et al (2014) Biochemical characterization and crystal structures of a fungal family 3 β-glucosidase, Cel3A from Hypocrea jecorina. J Biol Chem 289(45):31624–31637

    Article  Google Scholar 

  • Karlsson J, Saloheimo M, Siika-Aho M et al (2001) Homologous expression and characterization of Cel61A of Trichoderma reesei (EGIV). Eur J Biochem 268:6498–6507

    Article  Google Scholar 

  • Khademi S, Zhang D, Swanson SM et al (2002) Determination of the structure of an endoglucanase from Aspergillus niger and its mode of inhibition by palladium chloride. Acta Crystallogr D Biol Crystallogr 58(4):660–666

    Article  Google Scholar 

  • Kittl R, Kracher D, Burgstaller D et al (2012) Production of four Neurospora crassa lytic polysaccharide monooxygenases in Pichia pastoris monitored by a fluorimetric assay. Biotechnol Biofuels 5(1):79

    Article  Google Scholar 

  • Langston JA, Shaghasi T, Abbate E et al (2011) Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl Environ Microbiol 77(19):7007–7015

    Article  Google Scholar 

  • Lee TM, Farrow MF, Arnold FH et al (2011) A structural study of Hypocrea jecorina Cel5A. Prot Science 20:1935–1940

    Article  Google Scholar 

  • Levasseur A, Drula E, Lombard V et al (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6(1):41

    Article  Google Scholar 

  • Li X, Beeson WT 4th, Phillips CM et al (2012) Structural basis for substrate targeting and catalysis by fungal polysaccharide monooxygenases. Structure 20(6):1051–1061

    Article  Google Scholar 

  • Liu X, Ma Y, Zhang M (2015) Research advances in expansins and expansion-like proteins involved in lignocellulose degradation. Biotechnol Lett 37(8):1541–1551

    Article  MathSciNet  Google Scholar 

  • Lo Leggio L, Simmons TJ, Poulsen JC et al (2015) Structure and boosting activity of a starch-degrading lytic polysaccharide monooxygenase. Nat Commun 6:5961

    Article  Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E et al (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42(D1):D490–D495

    Article  Google Scholar 

  • Martinez D, Berka RM, Henrissat B et al (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26(5):553–560

    Article  Google Scholar 

  • Martinez D, Challacombe J, Morgenstern I et al (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci (USA) 106(6):1954–1959

    Article  Google Scholar 

  • McQueen-Mason S, Cosgrove DJ (1994) Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci (USA) 91(14):6574–6578

    Article  Google Scholar 

  • Medve J, Karlsson J, Lee D et al (1998) Hydrolysis of microcrystalline cellulose by cellobiohydrolase I and endoglucanase II from Trichoderma reesei: adsorption, sugar production pattern, and synergism of the enzymes. Biotechnol Bioeng 59(5):621–634

    Article  Google Scholar 

  • Mikkelsen D, Flanagan BM, Wilson SM et al (2015) Interactions of arabinoxylan and (1,3)(1,4)-β-glucan with cellulose networks. Biomacromol 16(4):1232–1239

    Article  Google Scholar 

  • Munoz IG, Ubhayasekera W, Henriksson H et al (2001) Family 7 cellobiohydrolases from Phanerochaete chrysosporium: crystal structure of the catalytic module of Cel7D (CBH58) at 1.32 Å resolution and homology models of the isozymes. J Mol Biol 314:1097

    Article  Google Scholar 

  • Navarro D, Rosso MN, Haon M et al (2014) Fast solubilization of recalcitrant cellulosic biomass by the basidiomycete fungus Laetisaria arvalis involves successive secretion of oxidative and hydrolytic enzymes. Biotechnol Biofuels 7(1):143

    Article  Google Scholar 

  • Payne CM, Knott BC, Mayes HB et al (2015) Fungal cellulases. Chem Rev 115(3):1308–1448

    Article  Google Scholar 

  • Phillips CM, Beeson WT, Cate JH et al (2011) Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. ACS Chem Biol 6(12):1399–1406

    Article  Google Scholar 

  • Poidevin L, Berrin JG, Bennati-Granier C et al (2014) Comparative analyses of Podospora anserina secretomes reveal a large array of lignocellulose-active enzymes. Appl Microbiol Biotechnol 98(17):7457–7469

    Article  Google Scholar 

  • Quinlan RJ, Sweeney MD, Lo Leggio L et al (2011) Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci USA 108(37):15079–15084

    Article  Google Scholar 

  • Quiroz-Castañeda RE, Martínez-Anaya C, Cuervo-Soto LI et al (2011) Loosenin, a novel protein with cellulose-disrupting activity from Bjerkandera adusta. Microb Cell Fact 10:8

    Article  Google Scholar 

  • Rahikainen JL, Martin-Sampedro R, Heikkinen H et al (2013) Inhibitory effect of lignin during cellulose bioconversion: the effect of lignin chemistry on non-productive enzyme adsorption. Biores Technol 133:270–278

    Article  Google Scholar 

  • Riley R, Salamov AA, Brown DW et al (2014) Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci USA 111(27):9923–9928

    Article  Google Scholar 

  • Saloheimo M, Nakari-Setälä T, Tenkanen M et al (1997) cDNA cloning of a Trichoderma reesei cellulase and demonstration of endoglucanase activity by expression in yeast. Eur J Biochem 249(2):584–591

    Article  Google Scholar 

  • Saloheimo M, Paloheimo M, Hakola S et al (2002) Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur J Biochem 269(17):4202–4211

    Article  Google Scholar 

  • Selig MJ, Knoshaug EP, Adney WS et al (2008) Synergistic enhancement of cellobiohydrolase performance on pretreated corn stover by addition of xylanase and esterase activities. Biores Technol 99(11):4997–5005

    Article  Google Scholar 

  • Sigoillot JC, Berrin JG, Bey M et al (2012) Fungal strategies for lignin degradation. In: Jouanin L, Lapierre C (eds) Advances in botanical research. Elsevier, Amsterdam, pp 263–308

    Google Scholar 

  • Tabka MG, Herpoël-Gimbert I, Monod F et al (2006) Enzymatic saccharification of wheat straw for bioethanol production by a combined cellulase xylanase and feruloyl esterase treatment. Enzyme Microb Technol 39(4):897–902

    Article  Google Scholar 

  • Tamura M, Miyazaki T, Tanaka Y et al (2012) Comparison of the structural changes in two cellobiohydrolases, CcCel6A and CcCel6C, from Coprinopsis cinerea—a tweezer-like motion in the structure of CcCel6C. FEBS J 279:1871–1882

    Article  Google Scholar 

  • Teugjas H, Väljamäe P (2013) Product inhibition of cellulases studied with 14C-labeled cellulose substrates. Biotechnol Biofuels 6(1):104

    Article  Google Scholar 

  • Tovar-Herrera OE, Batista-García RA, Sánchez-Carbente Mdel R et al (2015) A novel expansin protein from the white-rot fungus Schizophyllum commune. PLoS ONE 10(3):e0122296

    Article  Google Scholar 

  • Vaaje-Kolstad G, Horn SJ, van Aalten DM et al (2005) The non-catalytic chitin-binding protein CBP21 from Serratia marcescens is essential for chitin degradation. J Biol Chem 280(31):28492–28497

    Article  Google Scholar 

  • Vaaje-Kolstad G, Westereng B, Horn SJ et al (2010) An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330(6001):219–222

    Article  Google Scholar 

  • Várnai A, Mäkelä MR, Djajadi DT et al (2014) Carbohydrate-binding modules of fungal cellulases: occurrence in nature, function, and relevance in industrial biomass conversion. Adv Appl Microbiol 88:103–165

    Article  Google Scholar 

  • Vu V, Beeson WT, Span EA et al (2014a) A family of starch-active polysaccharide monooxygenases. Proc Natl Acad Sci USA 111(38):13822–13827

    Article  Google Scholar 

  • Vu V, Beeson WT, Phillips CM et al (2014b) Determinants of regioselective hydroxylation in the fungal polysaccharide monooxygenases. J Am Chem Soc 136(2):562–565

    Article  Google Scholar 

  • Wang T, Park YB, Cosgrove DJ et al (2015) Cellulose-pectin spatial contacts are inherent to never-dried Arabidopsis thaliana primary cell walls: evidence from solid-state NMR. Plant Physiol 168(3):871–884

    Article  Google Scholar 

  • Wood TM (1985) Properties of cellulolytic enzyme systems. Biochem Soc Trans 13(2):407–410

    Article  Google Scholar 

  • Wu M, Beckham GT, Larsson AM et al (2013) Crystal structure and computational characterization of the lytic polysaccharide monooxygenase GH61D from the basidiomycota fungus Phanerochaete chrysosporium. J Biol Chem 288(18):12828–12839

    Article  Google Scholar 

  • Zhang J, Pakarinen A, Viikari L (2013) Synergy between cellulases and pectinases in the hydrolysis of hemp. Biores Technol 129:302–307

    Article  Google Scholar 

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Couturier, M., Bennati-Granier, C., Urio, M.B., Ramos, L.P., Berrin, JG. (2016). Fungal Enzymatic Degradation of Cellulose. In: Soccol, C., Brar, S., Faulds, C., Ramos, L. (eds) Green Fuels Technology. Green Energy and Technology. Springer, Cham. https://doi.org/10.1007/978-3-319-30205-8_6

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