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Synergistic proteins for the enhanced enzymatic hydrolysis of cellulose by cellulase

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Abstract

Reducing the enzyme loadings for enzymatic saccharification of lignocellulose is required for economically feasible production of biofuels and biochemicals. One strategy is addition of small amounts of synergistic proteins to cellulase mixtures. Synergistic proteins increase the activity of cellulase without causing significant hydrolysis of cellulose. Synergistic proteins exert their activity by inducing structural modifications in cellulose. Recently, synergistic proteins from various biological sources, including bacteria, fungi, and plants, were identified based on genomic data, and their synergistic activities were investigated. Currently, an up-to-date overview of several aspects of synergistic proteins, such as their functions, action mechanisms and synergistic activity, are important for future industrial application. In this review, we summarize the current state of research on four synergistic proteins: carbohydrate-binding modules, plant expansins, expansin-like proteins, and Auxiliary Activity family 9 (formerly GH61) proteins. This review provides critical information to aid in promoting research on the development of efficient and industrially feasible synergistic proteins.

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References

  • Ali MK, Hayashi H, Karita S, Goto M, Kimura T, Sakka K, Ohmiya K (2001) Importance of the carbohydrate-binding module of Clostridium stercorarium Xyn10B to xylan hydrolysis. Biosci Biotechnol Biochem 65:41–47

    PubMed  CAS  Google Scholar 

  • Almeida JRM, Modig T, Petersson A, Hähn-Hägerdal B, Lidén G, Gorwa-Grauslund MF (2007) Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J Chem Technol Biotechnol 82:340–349

    CAS  Google Scholar 

  • Araki R, Ali MK, Sakka M, Kimura T, Sakka K, Ohmiya K (2004) Essential role of the family-22 carbohydrate-binding modules for β-1,3-1,4-glucanase activity of Clostridium stercorarium Xyn10B. FEBS Lett 561:155–158

    PubMed  CAS  Google Scholar 

  • Arantes V, Saddler JN (2010) Access to cellulose limits the efficiency of enzymatic hydrolysis: the role of amorphogenesis. Biotechnol Biofuels 3:4

    PubMed  PubMed Central  Google Scholar 

  • Baker J, King M, Adney W, Decker S, Vinzant T, Lantz S, Nieves R, Thomas S, Li L-C, Cosgrove D, Himmel M (2000) Investigation of the cell-wall loosening protein expansin as a possible additive in the enzymatic saccharification of lignocellulosic biomass. Appl Biochem Biotechnol 84–86:217–223

    PubMed  Google Scholar 

  • Banerjee G, Car S, Scott-Craig JS, Borrusch MS, Walton JD (2010) Rapid optimization of enzyme mixtures for deconstruction of diverse pretreatment/biomass feedstock combinations. Biotechnol Biofuels 3:22

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Berlin A, Gilkes N, Kurabi A, Bura R, Tu M, Kilburn D, Saddler J (2005) Weak lignin-binding enzymes: a novel approach to improve activity of cellulases for hydrolysis of lignocellulosics. Appl Biochem Biotechnol 121–124:163–170

    PubMed  Google Scholar 

  • Berlin A, Maximenko V, Gilkes N, Saddler J (2007) Optimization of enzyme complexes for lignocellulose hydrolysis. Biotechnol Bioeng 97:287–296

    PubMed  CAS  Google Scholar 

  • Bey M, Zhou SM, Poidevin L, Henrissat B, Coutinho PM, Berrin JG, Sigoillot JC (2013) Cello-oligosaccharide oxidation reveals differences between two lytic polysaccharide monooxygenases (family GH61) from Podospora anserina. Appl Environ Microbiol 79:488–496

    PubMed  CAS  PubMed Central  Google Scholar 

  • Boraston AB, Kwan E, Chiu P, Warren RA, Kilburn DG (2003) Recognition and hydrolysis of noncrystalline cellulose. J Biol Chem 278:6120–6127

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Brethauer S, Studer MH, Yang B, Wyman CE (2011) The effect of bovine serum albumin on batch and continuous enzymatic cellulose hydrolysis mixed by stirring or shaking. Bioresour Technol 102:6295–6298

    PubMed  CAS  Google Scholar 

  • Brotman Y, Briff E, Viterbo A, Chet I (2008) Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol 147:779–789

    PubMed  CAS  PubMed Central  Google Scholar 

  • Brummell DA, Harpster MH, Civello PM, Palys JM, Bennett AB, Dunsmuir P (1999) Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 11:2203–2216

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cannella D, C-w H, Felby C, Jorgensen H (2012) Production and effect of aldonic acids during enzymatic hydrolysis of lignocellulose at high dry matter content. Biotechnol Biofuels 5:26

    PubMed  CAS  PubMed Central  Google Scholar 

  • Chen X-a, Ishida N, Todaka N, Nakamura R, Maruyama J-i, Takahashi H, Kitamoto K (2010) Promotion of efficient saccharification of crystalline cellulose by Aspergillus fumigatus Swo1. Appl Environ Microbiol 76:2556–2561

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cho H-T, Cosgrove DJ (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci U S A 97:9783–9788

    PubMed  CAS  PubMed Central  Google Scholar 

  • Choi D, Lee Y, Cho H-T, Kende H (2003) Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15:1386–1398

    PubMed  CAS  PubMed Central  Google Scholar 

  • Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321–326

    PubMed  CAS  Google Scholar 

  • Cosgrove DJ (2001) Enhancement of accessibility of cellulose by expansins. US Patent 6326470

  • Cosgrove DJ, Bedinger P, Durachko DM (1997) Group I allergens of grass pollen as cell wall-loosening agents. Proc Natl Acad Sci U S A 94:6559–6564

    PubMed  CAS  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Din N, Gilkes NR, Tekant B, Miller RC, Warren AJ, Kilburn DG (1991) Non-hydrolytic disruption of cellulose fibers by the binding domain of a bacterial cellulase. BioTechnol 9:1096–1099

    CAS  Google Scholar 

  • Din N, Damude HG, Gilkes NR, Miller RC, Warren RAJ, Kilburn DG (1994) C1-Cx revisited—intramolecular synergism in a cellulase. Proc Natl Acad Sci U S A 91:11383–11387

    PubMed  CAS  PubMed Central  Google Scholar 

  • Forsberg Z, Vaaje-Kolstad G, Westereng B, Bunaes AC, Stenstrom Y, MacKenzie A, Sorlie M, Horn SJ, Eijsink VGH (2011) Cleavage of cellulose by a CBM33 protein. Protein Sci 20:1479–1483

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gao PJ, Chen GJ, Wang TH, Zhang YS, Liu J (2001) Non-hydrolytic disruption of crystalline structure of cellulose by cellulose binding domain and linker sequence of cellobiohydrolase I from Penicillium janthinellum. Acta Biochim Biophys Sin 33:13–18

    PubMed  CAS  Google Scholar 

  • Gao D, Chundawat SPS, Krishnan C, Balan V, Dale BE (2010) Mixture optimization of six core glycosyl hydrolases for maximizing saccharification of ammonia fiber expansion (AFEX) pretreated corn stover. Bioresour Technol 101:2770–2781

    PubMed  CAS  Google Scholar 

  • Garvey M, Klose H, Fischer R, Lambertz C, Commandeur U (2013) Cellulases for biomass degradation: comparing recombinant cellulase expression platforms. Trends Biotechnol 31:581–593

    PubMed  CAS  Google Scholar 

  • Georgelis N, Tabuchi A, Nikolaidis N, Cosgrove DJ (2011) Structure-function analysis of the bacterial expansin EXLX1. J Biol Chem 286:16814–16823

    PubMed  CAS  PubMed Central  Google Scholar 

  • Georgelis N, Yennawar NH, Cosgrove DJ (2012) Structural basis for entropy-driven cellulose binding by a type-A cellulose-binding module (CBM) and bacterial expansin. Proc Natl Acad Sci U S A 109:14830–14835

    PubMed  CAS  PubMed Central  Google Scholar 

  • Georgelis N, Nikolaidis N, Cosgrove DJ (2014) Biochemical analysis of expansin-like proteins from microbes. Carbohydr Polym 100:17–23

    PubMed  CAS  Google Scholar 

  • Gilkes NR, Henrissat B, Kilburn DG, Miller RC Jr, Warren RA (1991) Domains in microbial ß-1,4-glycanases: sequence conservation, function, and enzyme families. Microbiol Rev 55:303–315

    PubMed  CAS  PubMed Central  Google Scholar 

  • Gilligan W, Reese ET (1954) Evidence for multiple components in microbial cellulases. Can J Microbiol 1:90–107

    PubMed  CAS  Google Scholar 

  • Hall M, Bansal P, Lee JH, Realff MJ, Bommarius AS (2011) Biological pretreatment of cellulose: enhancing enzymatic hydrolysis rate using cellulose-binding domains from cellulases. Bioresour Technol 102:2910–2915

    PubMed  CAS  Google Scholar 

  • Harris PV, Welner D, McFarland KC, Re E, Poulsen JCN, Brown K, Salbo R, Ding HS, Vlasenko E, Merino S, Xu F, Cherry J, Larsen S, Lo Leggio L (2010) Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: structure and function of a large, enigmatic family. Biochemistry 49:3305–3316

    PubMed  CAS  Google Scholar 

  • Hess M (2008) Thermoacidophilic proteins for biofuel production. Trends Microbiol 16:414–419

    PubMed  CAS  Google Scholar 

  • Himmel ME, Ding S-Y, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315:804–807

    PubMed  CAS  Google Scholar 

  • Jäger G, Girfoglio M, Dollo F, Rinaldi R, Bongard H, Commandeur U, Fischer R, Spiess A, Buchs J (2011) How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis. Biotechnol Biofuels 4:33

    PubMed  PubMed Central  Google Scholar 

  • Jalak J, Kurašin M, Teugjas H, Väljamäe P (2012) Endo-exo synergism in cellulose hydrolysis revisited. J Biol Chem 287:28802–28815

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jung YH, Kim S, Yang TH, Lee HJ, Seung D, Park YC, Seo JH, Choi I-G, Kim KH (2012) Aqueous ammonia pretreatment, saccharification, and fermentation evaluation of oil palm fronds for ethanol production. Bioprocess Biosyst Eng 35:1497–1503

    PubMed  CAS  Google Scholar 

  • Kang K, Wang S, Lai G, Liu G, Xing M (2013) Characterization of a novel swollenin from Penicillium oxalicum in facilitating enzymatic saccharification of cellulose. BMC Biotechnol 13:42

    PubMed  CAS  PubMed Central  Google Scholar 

  • Karkehabadi S, Hansson H, Kim S, Piens K, Mitchinson C, Sandgren M (2008) The first structure of a glycoside hydrolase family 61 member, Cel61B from Hypocrea jecorina, at 1.6 angstrom resolution. J Mol Biol 383:144–154

    PubMed  CAS  Google Scholar 

  • Kende H, Bradford K, Brummell D, Cho H-T, Cosgrove D, Fleming A, Gehring C, Lee Y, McQueen-Mason S, Rose J, Voesenek L (2004) Nomenclature for members of the expansin superfamily of genes and proteins. Plant Mol Biol 55:311–314

    PubMed  CAS  Google Scholar 

  • Kerff F, Amoroso A, Herman R, Sauvage E, Petrella S, Filée P, Charlier P, Joris B, Tabuchi A, Nikolaidis N, Cosgrove DJ (2008) Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization. Proc Natl Acad Sci U S A 105:16876–16881

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kim ES, Lee HJ, Bang W-G, Choi I-G, Kim KH (2009) Functional characterization of a bacterial expansin from Bacillus subtilis for enhanced enzymatic hydrolysis of cellulose. Biotechnol Bioeng 102:1342–1353

    PubMed  CAS  Google Scholar 

  • Kim T-W, Chokhawala HA, Hess M, Dana CM, Baer Z, Sczyrba A, Rubin EM, Blanch HW, Clark DS (2011) High-throughput in vitro glycoside hydrolase (HIGH) screening for enzyme discovery. Angew Chem Int Ed Engl 50:11215–11218

    PubMed  CAS  Google Scholar 

  • Kim IJ, Ko HJ, Kim TW, Choi I-G, Kim KH (2013a) Characteristics of the binding of a bacterial expansin (BsEXLX1) to microcrystalline cellulose. Biotechnol Bioeng 110:401–407

    PubMed  CAS  Google Scholar 

  • Kim IJ, Ko HJ, Kim TW, Nam KH, Choi I-G, Kim KH (2013b) Binding characteristics of a bacterial expansin (BsEXLX1) for various types of pretreated lignocellulose. Appl Microbiol Biotechnol 97:5381–5388

    PubMed  CAS  Google Scholar 

  • Koseki T, Mese Y, Fushinobu S, Masaki K, Fujii T, Ito K, Shiono Y, Murayama T, Iefuji H (2008) Biochemical characterization of a glycoside hydrolase family 61 endoglucanase from Aspergillus kawachii. Appl Microbiol Biotechnol 77:1279–1285

    PubMed  CAS  Google Scholar 

  • Kostylev M, Wilson D (2011) Synergistic interactions in cellulose hydrolysis. Biofuels 3:61–70

    Google Scholar 

  • Kumar R, Wyman CE (2009) Does change in accessibility with conversion depend on both the substrate and pretreatment technology? Bioresour Technol 100:4193–4202

    PubMed  CAS  Google Scholar 

  • Laine MJ, Haapalainen M, Wahlroos T, Kankare K, Nissinen R, Kassuwi S, Metzler MC (2000) The cellulase encoded by the native plasmid of Clavibacter michiganensis ssp. sepedonicus plays a role in virulence and contains an expansin-like domain. Physiol Mol Plant P 57:221–233

    CAS  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Le Costaouëc T, Pakarinen A, Várnai A, Puranen T, Viikari L (2013) The role of carbohydrate binding module (CBM) at high substrate consistency: comparison of Trichoderma reesei and Thermoascus aurantiacus Cel7A (CBHI) and Cel5A (EGII). Bioresour Technol 143:196–203

    PubMed  Google Scholar 

  • Lee HJ, Lee S, Ko HJ, Kim KH, Choi I-G (2010) An expansin-like protein from Hahella chejuensis binds cellulose and enhances cellulase activity. Mol Cells 29:379–385

    PubMed  CAS  Google Scholar 

  • Lee HJ, Kim IJ, Kim JF, Choi I-G, Kim KH (2013) An expansin from the marine bacterium Hahella chejuensis acts synergistically with xylanase and enhances xylan hydrolysis. Bioresour Technol 149:516–519

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Li X, Beeson WT, Phillips CM, Marletta MA, Cate JHD (2012) Structural basis for substrate targeting and catalysis by fungal polysaccharide monooxygenases. Structure 20:1051–1061

    PubMed  PubMed Central  Google Scholar 

  • Lin H, Shen Q, Zhan J-M, Wang Q, Zhao Y-H (2013) Evaluation of bacterial expansin EXLX1 as a cellulase synergist for the saccharification of lignocellulosic agro-industrial wastes. PLoS One 8:e75022

    PubMed  CAS  PubMed Central  Google Scholar 

  • Lynd LR, Zyl WH, McBride JE, Laser M (2005) Consolidated bioprocessing of cellulosic biomass: an update. Curr Opin Biotechnol 16:577–583

    PubMed  CAS  Google Scholar 

  • Lynd LR, Laser MS, Brandsby D, Dale BE, Davison B, Hamilton R, Himmel M, Keller M, McMillan JD, Sheehan J, Wyman CE (2008) How biotech can transform biofuels. Nat Biotechnol 26:169–172

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  PubMed Central  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 U S A 91:6574–6578

    PubMed  CAS  PubMed Central  Google Scholar 

  • McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–1433

    PubMed  CAS  PubMed Central  Google Scholar 

  • Merino ST, Cherry J (2007) Progress and challenges in enzyme development for biomass utilization. Adv Biochem Eng Biotechnol 108:95–120

    PubMed  CAS  Google Scholar 

  • Nakatani Y, Yamada R, Ogino C, Kondo A (2013) Synergetic effect of yeast cell-surface expression of cellulase and expansin-like protein on direct ethanol production from cellulose. Microb Cell Fact 12:66

    PubMed  CAS  PubMed Central  Google Scholar 

  • Nikolaidis N, Doran N, Cosgrove DJ (2013) Plant expansins in bacteria and fungi: evolution by horizontal gene transfer and independent domain fusion. Mol Biol Evol 31:498

    Google Scholar 

  • Pakarinen A, Haven M, Djajadi D, Varnai A, Puranen T, Viikari L (2014) Cellulases without carbohydrate-binding modules in high consistency ethanol production process. Biotechnol Biofuels 7:27

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Pien S, Wyrzykowska J, McQueen-Mason S, Smart C, Fleming A (2001) Local expression of expansin induces the entire process of leaf development and modifies leaf shape. Proc Nat Acad Sci 98:11812–11817

    PubMed  CAS  PubMed Central  Google Scholar 

  • Pu Y, Hu F, Huang F, Davison BH, Ragauskas AJ (2013) Assessing the molecular structure basis for biomass recalcitrance during dilute acid and hydrothermal pretreatments. Biotechnol Biofuels 6:15

    PubMed  CAS  PubMed Central  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Reese ET, Siu RGH, Levinson HS (1950) The biological degradation of soluble cellulose derivatives and its relationship to the mechanism of cellulose hydrolysis. J Bacteriol 59:485–497

    PubMed  CAS  PubMed Central  Google Scholar 

  • Reinikainen T, Ruohonen L, Nevanen T, Laaksonen L, Kraulis P, Jones TA, Knowles JK, Teeri TT (1992) Investigation of the function of mutated cellulose-binding domains of Trichoderma reesei cellobiohydrolase I. Proteins 14:475–482

    PubMed  CAS  Google Scholar 

  • Rodríguez-Sanoja R, Ruiz B, Guyot JP, Sanchez S (2005) Starch-binding domain affects catalysis in two Lactobacillus α-amylases. Appl Environ Microbiol 71:297–302

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B, Nyyssönen E, Bhatia A, Ward M, Penttilä M (2002) Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur J Biochem 269:4202–4211

    PubMed  CAS  Google Scholar 

  • Shao W, Wiegel J (1995) Purification and characterization of two thermostable acetyl xylan esterases from Thermoanaerobacterium sp. strain JW/SL-YS485. Appl Environ Microbiol 61:729–733

    PubMed  CAS  PubMed Central  Google Scholar 

  • Shieh MW, Cosgrove DJ (1998) Expansins. J Plant Res 111:149–157

    PubMed  CAS  Google Scholar 

  • Shoseyov O, Shani Z, Levy I (2006) Carbohydrate binding modules: biochemical properties and novel applications. Microbiol Mol Biol R 70:283–295

    CAS  Google Scholar 

  • StÅHlberg J, Johansson G, Pettersson G (1988) A binding site-deficient, catalytically active, core protein of endoglucanase III from the culture filtrate of Trichoderma reesei. Eur J Biochem 173:179–183

    PubMed  Google Scholar 

  • Suwannarangsee S, Bunterngsook B, Arnthong J, Paemanee A, Thamchaipenet A, Eurwilaichitr L, Laosiripojana N, Champreda V (2012) Optimisation of synergistic biomass-degrading enzyme systems for efficient rice straw hydrolysis using an experimental mixture design. Bioresour Technol 119:252–261

    PubMed  CAS  Google Scholar 

  • Tian C, Beeson WT, Iavarone AT, Sun J, Marletta MA, Cate JHD, Glass NL (2009) Systems analysis of plant cell wall degradation by the model filamentous fungus Neurospora crassa. Proc Natl Acad Sci U S A 106:22157–22162

    PubMed  CAS  PubMed Central  Google Scholar 

  • Tomme P, Van Tilbeurgh H, Pettersson G, Van Damme J, Vandekerckhove J, Knowles J, Teeri T, Claeyssens M (1988) Studies of the cellulolytic system of Trichoderma reesei QM 9414. Eur J Biochem 170:575–581

    PubMed  CAS  Google Scholar 

  • Um BH, Hanley TR (2008) High-solid enzymatic hydrolysis and fermentation of solka floc into ethanol. J Microbiol Biotechnol 18:1257–1265

    PubMed  CAS  Google Scholar 

  • Um BH, van Walsum GP (2012) Effect of pretreatment severity on accumulation of major degradation products from dilute acid pretreated corn stover and subsequent inhibition of enzymatic hydrolysis of cellulose. Appl Biochem Biotechnol 168:406–420

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Vaaje-Kolstad G, Westereng B, Horn SJ, Liu ZL, Zhai H, Sorlie M, Eijsink VGH (2010) An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330:219–222

    PubMed  CAS  Google Scholar 

  • van Walsum GP, Shi H (2004) Carbonic acid enhancement of hydrolysis in aqueous pretreatment of corn stover. Bioresour Technol 93:217–226

    PubMed  Google Scholar 

  • Várnai A, Siika-aho M, Viikari L (2013) Carbohydrate-binding modules (CBMs) revisited: reduced amount of water counterbalances the need for CBMs. Biotechnol Biofuels 6:30

    PubMed  PubMed Central  Google Scholar 

  • Viikari L, Alapuranen M, Puranen T, Vehmaanpera J, Siika-Aho M (2007) Thermostable enzymes in lignocellulose hydrolysis. Adv Biochem Eng Biotechnol 108:121–145

    PubMed  CAS  Google Scholar 

  • Wang M, Cai J, Huang L, Lv Z, Zhang Y, Xu Z (2010) High-level expression and efficient purification of bioactive swollenin in Aspergillus oryzae. Appl Biochem Biotechnol 162:2027–2036

    PubMed  CAS  Google Scholar 

  • Wang Y, Tang R, Tao J, Gao G, Wang X, Mu Y, Feng Y (2011) Quantitative investigation of non-hydrolytic disruptive activity on crystalline cellulose and application to recombinant swollenin. Appl Microbiol Biotechnol 91:1353–1363

    PubMed  CAS  Google Scholar 

  • Wang W, Liu C, Ma Y, Liu X, Zhang K, Zhang M (2014) Improved production of two expansin-like proteins in Pichia pastoris and investigation of their functional properties. Biochem Eng J 84:16–27

    CAS  Google Scholar 

  • Watson BJ, Zhang H, Longmire AG, Moon YH, Hutcheson SW (2009) Processive endoglucanases mediate degradation of cellulose by Saccharophagus degradans. J Bacteriol 191:5697–5705

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wei W, Yang C, Luo J, Lu C, Wu Y, Yuan S (2010) Synergism between cucumber α-expansin, fungal endoglucanase and pectin lyase. J Plant Physiol 167:1204–1210

    PubMed  CAS  Google Scholar 

  • Westereng B, Ishida T, Vaaje-Kolstad G, Wu M, Eijsink VGH, Igarashi K, Samejima M, Stahlberg J, Horn SJ, Sandgren M (2011) The putative endoglucanase PcGH61D from Phanerochaete chrysosporium is a metal-dependent oxidative enzyme that cleaves cellulose. PLoS One 6(11):e27807

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wu M, Beckham GT, Larsson AM, Ishida T, Kim S, Payne CM, Himmel ME, Crowley MF, Horn SJ, Westereng B, Igarashi K, Samejima M, Stahlberg J, Eijsink VGH, Sandgren M (2013) Crystal structure and computational characterization of the lytic polysaccharide monooxygenase GH61D from the basidiomycota fungus Phanerochaete chrysosporium. J Biol Chem 288:12828–12839

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yang B, Wyman CE (2006) BSA treatment to enhance enzymatic hydrolysis of cellulose in lignin containing substrates. Biotechnol Bioeng 94:611–617

    PubMed  CAS  Google Scholar 

  • Yennawar NH, Li LC, Dudzinski DM, Tabuchi A, Cosgrove DJ (2006) Crystal structure and activities of EXPB1 (Zea m 1), a β-expansin and group-1 pollen allergen from maize. Proc Natl Acad Sci U S A 103:14664–14671

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yeoman CJ, Han Y, Dodd D, Schroeder CM, Mackie RI, Cann IK (2010) Thermostable enzymes as biocatalysts in the biofuel industry. Adv Appl Microbiol 70:1–55

    PubMed  CAS  Google Scholar 

  • Zhou QX, Lv XX, Zhang X, Meng XF, Chen GJ, Liu WF (2011) Evaluation of swollenin from Trichoderma pseudokoningii as a potential synergistic factor in the enzymatic hydrolysis of cellulose with low cellulase loadings. World J Microbiol Biotechnol 27:1905–1910

    CAS  Google Scholar 

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Acknowledgments

This work was supported by grants from the National Research Foundation of Korea (2013M1A2A2072597) and the Advanced Biomass R&D Center of Korea (2011-0031353), both funded by the Korean Government (MSIP). This research was performed at the Korea University Food Safety Hall for the Institute of Biomedical Science and Food Safety.

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  1. Department of Biotechnology, Korea University Graduate School, Seoul, 136-713, Republic of Korea

    In Jung Kim, Hee Jin Lee, In-Geol Choi & Kyoung Heon Kim

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  1. In Jung Kim
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  2. Hee Jin Lee
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  3. In-Geol Choi
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  4. Kyoung Heon Kim
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Correspondence to Kyoung Heon Kim.

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Kim, I.J., Lee, H.J., Choi, IG. et al. Synergistic proteins for the enhanced enzymatic hydrolysis of cellulose by cellulase. Appl Microbiol Biotechnol 98, 8469–8480 (2014). https://doi.org/10.1007/s00253-014-6001-3

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  • DOI: https://doi.org/10.1007/s00253-014-6001-3

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