A mini review of xylanolytic enzymes with regards to their synergistic interactions during hetero-xylan degradation
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Abstract
This review examines the recent models describing the mode of action of various xylanolytic enzymes and how these enzymes can be applied (sequentially or simultaneously) with their distinctive roles in mind to achieve efficient xylan degradation. With respect to homeosynergy, synergism appears to be as a result of β-xylanase and/or oligosaccharide reducing-end β-xylanase liberating xylo-oligomers (XOS) that are preferred substrates of the processive β-xylosidase. With regards to hetero-synergism, two cross relationships appear to exist and seem to be the reason for synergism between the enzymes during xylan degradation. These cross relations are the debranching enzymes such as α-glucuronidase or side-chain cleaving enzymes such as carbohydrate esterases (CE) removing decorations that would have hindered back-bone-cleaving enzymes, while backbone-cleaving-enzymes liberate XOS that are preferred substrates of the debranching and side-chain-cleaving enzymes. This interaction is demonstrated by high yields in co-production of xylan substituents such as arabinose, glucuronic acid and ferulic acid, and XOS. Finally, lytic polysaccharide monooxygenases (LPMO) have also been implicated in boosting whole lignocellulosic biomass or insoluble xylan degradation by glycoside hydrolases (GH) by possibly disrupting entangled xylan residues. Since it has been observed that the same enzyme (same Enzyme Commission, EC, classification) from different GH or CE and/or AA families can display different synergistic interactions with other enzymes due to different substrate specificities and properties, in this review, we propose an approach of enzyme selection (and mode of application thereof) during xylan degradation, as this can improve the economic viability of the degradation of xylan for producing precursors of value added products.
Keywords
Carbohydrate esterases Degradation Glycoside hydrolases Lytic polysaccharide monooxygenase Synergy XylanAbbreviations
- AA
Auxiliary activity
- Abf
α-Arabinofuranosidase
- Agu
α-Glucuronidase
- AGX
Arabinoglucuronoxylan
- AX
Arabinoxylan
- AXE
Acetyl xylan esterase
- AXH-d
Doubly substituted L-Araf specific α-arabinofuranosidase
- AXH-m
Mono-substituted L-Araf specific α-arabinofuranosidase
- CAZy
Carbohydrate active enzyme database
- CAZyme
Carbohydrate-active enzyme
- CE
Carbohydrate esterase
- DS
Degree of synergy
- EC
Enzyme commission number
- FA
Ferulic acid
- FAE
Feruloyl esterase
- GE
Glucuronoyl esterase
- GH
Glycoside hydrolase
- GX
Glucuronoxylan
- LPMO
Lytic polysaccharide mono-oxygenase
- Rex
Oligosaccharide reducing-end xylanase
- RS
Reducing sugar(s)
- XOS
Xylo-oligosaccharide(s)
- Xyn
β-Xylanase
- Xyl
β-Xylosidase
Notes
Compliance with ethical standards
Conflict of interest
The authors report no further conflicts of interest. The authors are responsible for the content and writing of this article and are grateful for financial support from the National Research Foundation (NRF) and Council for Scientific and Industrial Research (CSIR) in South Africa. Any opinion, findings and conclusions or recommendations expressed in this material are those of the author(s) and therefore the NRF does not accept any liability in regard thereto.
References
- Adesioye FA, Makhalanyane TP, Biely P, Cowan DA (2016) Phylogeny, classification and metagenomic bioprospecting of microbial acetyl xylan esterases. Enzyme Microb Technol 93–94:79–91PubMedCrossRefGoogle Scholar
- Adesioye FA, Makhalanyane TP, Vikram S et al (2018) Structural characterization and directed evolution of a novel acetyl xylan esterase reveals thermostability determinants of the carbohydrate esterase 7 family. Appl Environ Microbiol 84(8):e02695–e2717PubMedPubMedCentralCrossRefGoogle Scholar
- Arfi Y, Shamshoum M, Rogachev I et al (2014) Integration of bacterial lytic polysaccharide monooxygenases into designer cellulosomes promotes enhanced cellulose degradation. Proc Natl Acad Sci 111:9109–9114PubMedCrossRefGoogle Scholar
- Baath J, Giummarella N, Klaubauf S et al (2016) A glucuronoyl esterase from Acremonium alcalophilum cleaves native lignin-carbohydrate ester bonds. FEBS Lett 590:2611–2618CrossRefGoogle Scholar
- Banka AL, Albayrak Guralp S, Gulari E (2014) Secretory expression and characterization of two hemicellulases, xylanase, and beta-xylosidase, isolated from Bacillus subtilis M015. Appl Biochem Biotechnol 174:2702–2710PubMedPubMedCentralCrossRefGoogle Scholar
- Beaugrand J, Chambat G, Wong VWK et al (2004) Impact and efficiency of GH10 and GH11 thermostable endoxylanases on wheat bran and alkali-extractable arabinoxylans. Carbohydr Res 339:2529–2540PubMedCrossRefGoogle Scholar
- Biely P, MalovÓková A, Hirsch J et al (2015) The role of the glucuronoxylan carboxyl groups in the action of endoxylanases of three glycoside hydrolase families: a study with two substrate mutants. Biochim Biophys Acta - Gen Subj 1850:2246–2255CrossRefGoogle Scholar
- Biely P, Puchart V, Stringer MA, Mørkeberg Krogh KBR (2014) Trichoderma reesei XYN VI - A novel appendage-dependent eukaryotic glucuronoxylan hydrolase. FEBS J 281:3894–3903PubMedCrossRefGoogle Scholar
- Biely P, Singh S, Puchart V (2016) Towards enzymatic breakdown of complex plant xylan structures: state of the art. Biotechnol Adv 34(7):1260–1274PubMedCrossRefGoogle Scholar
- Broeker J, Mechelke M, Baudrexl M et al (2018) The hemicellulose-degrading enzyme system of the thermophilic bacterium Clostridium stercorarium: comparative characterisation and addition of new hemicellulolytic glycoside hydrolases. Biotechnol Biofuels 11(1):229PubMedPubMedCentralCrossRefGoogle Scholar
- Chadha BS, Kaur B, Basotra N et al (2019) Thermostable xylanases from thermophilic fungi and bacteria: current perspective. Bioresour Technol 277:195–203PubMedCrossRefGoogle Scholar
- Charoensiddhi S, Conlon MA, Franco CMM, Zhang W (2017) The development of seaweed-derived bioactive compounds for use as prebiotics and nutraceuticals using enzyme technologies. Trends Food Sci Technol 70:20–33CrossRefGoogle Scholar
- Choengpanya K, Arthornthurasuk S, Wattana-Amorn P et al (2015) Cloning, expression and characterization of β-xylosidase from Aspergillus Niger ASKU28. Protein Expr Purif 115:132–140PubMedCrossRefGoogle Scholar
- Christakopoulos P, Katapodis P, Kalogeris E et al (2003) Antimicrobial activity of acidic xylo-oligosaccharides produced by family 10 and 11 endoxylanases. Int J Biol Macromol 31:171–175PubMedCrossRefGoogle Scholar
- Cobucci-Ponzano B, Strazzulli A, Iacono R et al (2015) Novel thermophilic hemicellulases for the conversion of lignocellulose for second generation biorefineries. Enzyme Microb Technol 78:63–73PubMedCrossRefGoogle Scholar
- Collins T, Gerday C, Feller G (2005) Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol Rev 29:3–23PubMedCrossRefGoogle Scholar
- Corrêa LTR, Júnior AT, Wolf LD et al (2019) An actinobacteria lytic polysaccharide monooxygenase acts on both cellulose and xylan to boost biomass saccharification. Biotechnol Biofuels 12(1):117PubMedPubMedCentralCrossRefGoogle Scholar
- Couturier M, Ladevèze S, Sulzenbacher G et al (2018) Lytic xylan oxidases from wood-decay fungi unlock biomass degradation. Nat Chem Biol 14:306–310PubMedCrossRefGoogle Scholar
- Cragg SM, Beckham GT, Bruce NC et al (2015) Lignocellulose degradation mechanisms across the tree of life. Curr Opin Chem Biol 29:108–119CrossRefGoogle Scholar
- Ebringerová A (2006) Structural diversity and application potential of hemicelluloses. Macromol Symp 232:1–12CrossRefGoogle Scholar
- Faundez C, Perez R, Ravanal MC, Eyzaguirre J (2019) Penicillium purpurogenum produces a novel, acidic, GH3 beta-xylosidase: heterologous expression and characterization of the enzyme. Carbohydr Res 482:107728CrossRefGoogle Scholar
- Frommhagen M, Sforza S, Westphal AH et al (2015) Discovery of the combined oxidative cleavage of plant xylan and cellulose by a new fungal polysaccharide monooxygenase. Biotechnol Biofuels 8:101PubMedPubMedCentralCrossRefGoogle Scholar
- Ghio S, Ontañon O, Piccinni FE et al (2018) Paenibacillus sp. A59 GH10 and GH11 extracellular endoxylanases: application in biomass bioconversion. BioEnergy Res 11:174–190CrossRefGoogle Scholar
- Golan G, Shallom D, Teplitsky A et al (2004) Crystal structures of Geobacillus stearothermophilus alpha-glucuronidase complexed with its substrate and products: mechanistic implications. J Biol Chem 279:3014–3024PubMedCrossRefGoogle Scholar
- Goncalves GAL, Takasugi Y, Jia L et al (2015) Synergistic effect and application of xylanases as accessory enzymes to enhance the hydrolysis of pretreated bagasse. Enzyme Microb Technol 72:16–24PubMedCrossRefGoogle Scholar
- Guerfali M, Gargouri A, Belghith H (2011) Catalytic properties of Talaromyces thermophilus alpha-L- arabinofuranosidase and its synergistic action with immobilized endo-beta-1,4-xylanase. J Mol Catal B 68:192–199CrossRefGoogle Scholar
- Guo X, Zhang R, Li Z et al (2013) A novel pathway construction in Candida tropicalis for direct xylitol conversion from corncob xylan. Bioresour Technol 128:547–552PubMedCrossRefGoogle Scholar
- Hemsworth GR, Johnston EM, Davies GJ, Walton PH (2015) Lytic polysaccharide monooxygenases in biomass conversion. Trends Biotechnol 33(12):747–761PubMedPubMedCentralCrossRefGoogle Scholar
- Hettiarachchi SA, Kwon YK, Lee Y et al (2019) Characterization of an acetyl xylan esterase from the marine bacterium Ochrovirga pacifica and its synergism with xylanase on beechwood xylan. Microb Cell Fact 18:122PubMedPubMedCentralCrossRefGoogle Scholar
- Horn SJ, Vaaje-Kolstad G, Westereng B, Eijsink VG (2012) Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 5:45PubMedPubMedCentralCrossRefGoogle Scholar
- Hu J, Tian D, Renneckar S, Saddler JN (2018) Enzyme mediated nanofibrillation of cellulose by the synergistic actions of an endoglucanase, lytic polysaccharide monooxygenase (LPMO) and xylanase. Sci Rep 8:3195PubMedPubMedCentralCrossRefGoogle Scholar
- Huy ND, Le NC, Seo JW et al (2015) Putative endoglucanase PcGH5 from Phanerochaete chrysosporium is a beta-xylosidase that cleaves xylans in synergistic action with endo-xylanase. J Biosci Bioeng 119:416–420PubMedCrossRefGoogle Scholar
- Jamaldheen SB, Thakur A, Moholkar VS, Goyal A (2019) Enzymatic hydrolysis of hemicellulose from pretreated Finger millet (Eleusine coracana) straw by recombinant endo-1,4-beta-xylanase and exo-1,4-beta-xylosidase. Int J Biol Macromol 135:1098–1106PubMedCrossRefGoogle Scholar
- Jeffries TW (1990) Biodegradation of lignin-carbohydrate complexes. Biodegradation 1:163–176CrossRefGoogle Scholar
- Jia X, Mi S, Wang J et al (2014) Insight into glycoside hydrolases for debranched xylan degradation from extremely thermophilic bacterium Caldicellulosiruptor lactoaceticus. PLoS ONE 9:1–12Google Scholar
- Jung S, Song Y, Myeong H, Bae H (2015) Enhanced lignocellulosic biomass hydrolysis by oxidative lytic polysaccharide monooxygenases (LPMOs) GH61 from Gloeophyllum trabeum. Enzyme Microb Technol 77:38–45PubMedCrossRefGoogle Scholar
- Juturu V, Teh TM, Wu JC (2014) Expression of Aeromonas punctata ME-1 exo-xylanase X in E. coli for efficient hydrolysis of xylan to xylose. Appl Biochem Biotechnol 174:2653–2662PubMedCrossRefGoogle Scholar
- Juturu V, Wu JC (2012) Microbial xylanases: engineering, production and industrial applications. Biotechnol Adv 30:1219–1227PubMedCrossRefGoogle Scholar
- Kamat S, Khot M, Zinjarde S et al (2013) Coupled production of single cell oil as biodiesel feedstock, xylitol and xylanase from sugarcane bagasse in a biorefinery concept using fungi from the tropical mangrove wetlands. Bioresour Technol 135:246–253PubMedCrossRefGoogle Scholar
- Kambourova M, Mandeva R, Fiume I et al (2007) Hydrolysis of xylan at high temperature by co-action of the xylanase from Anoxybacillus flavithermus BC and the beta-xylosidase/alpha-arabinosidase from Sulfolobus solfataricus Oα. J Appl Microbiol 102:1586–1593PubMedCrossRefGoogle Scholar
- Kang Q, Appels L, Tan T, Dewil R (2014) Bioethanol from Lignocellulosic Biomass: Current Findings Determine Research Priorities. Sci World J. https://doi.org/10.1155/2014/298153 CrossRefGoogle Scholar
- Karlsson EN, Schmitz E, Linares-pastén JA, Adlercreutz P (2018) Endo-xylanases as tools for production of substituted xylooligosaccharides with prebiotic properties. Appl Microbiol Biotechnol 102:9081–9088CrossRefGoogle Scholar
- Kim IJ, Nam KH, Yun EJ et al (2015) Optimization of synergism of a recombinant auxiliary activity 9 from Chaetomium globosum with cellulase in cellulose hydrolysis. Appl Microbiol Biotechnol 99:8537–8547PubMedPubMedCentralCrossRefGoogle Scholar
- Kim IJ, Youn HJ, Kim KH (2016) Synergism of an auxiliary activity 9 (AA9) from Chaetomium globosum with xylanase on the hydrolysis of xylan and lignocellulose. Process Biochem 51:1445–1451CrossRefGoogle Scholar
- Knob A, Terrasan CRF, Carmona EC (2010) β-Xylosidases from filamentous fungi: an overview. World J Microbiol Biotechnol 26:389–407CrossRefGoogle Scholar
- Kormelink FJM, Voragen AGJ (1993) Degradation of different [(glucurono)arabino]xylans by a combination of purified xylan-degrading enzymes. Appl Microbiol Biotechnol 38:688–695CrossRefGoogle Scholar
- Kumar R, Wyman C (2009) Effects of cellulase and xylanase enzymes on the deconstruction of solids from pretreatment of poplar by leading technologies. Biotechnol Prog 25:302–314PubMedCrossRefGoogle Scholar
- Kumar V, Marín-Navarro J, Shukla P (2016) Thermostable microbial xylanases for pulp and paper industries: trends, applications and further perspectives. World J Microbiol Biotechnol 32:1–10CrossRefGoogle Scholar
- Lagaert S, Pollet A, Courtin CM, Volckaert G (2014) β-Xylosidases and α-L-arabinofuranosidases: accessory enzymes for arabinoxylan degradation. Biotechnol Adv 32:316–332PubMedCrossRefGoogle Scholar
- Lagaert S, Van Campenhout S, Pollet A et al (2007) Recombinant expression and characterization of a reducing-end xylose-releasing exo-oligoxylanase from Bifidobacterium adolescentis. Appl Environ Microbiol 73:5374–5377PubMedPubMedCentralCrossRefGoogle Scholar
- Lei Z, Shao Y, Yin X et al (2016) Combination of xylanase and debranching enzymes specific to wheat arabinoxylan improve the growth performance and gut health of broilers. J Agric Food Chem 64:4932–4942PubMedCrossRefGoogle Scholar
- Li K, Helm RF (1995) Synthesis and rearrangement reactions of ester-linked lignin-carbohydrate model compounds. J Agric Food Chem 43:2098–2103CrossRefGoogle Scholar
- Linder Å, Bergman R, Bodin A, Gatenholm P (2003) Mechanism of assembly of xylan onto cellulose surfaces. Langmuir 19:5072–5077CrossRefGoogle Scholar
- Liu X, Jiang Z, Liu Y et al (2019a) Biochemical characterization of a novel exo-oligoxylanase from Paenibacillus barengoltzii suitable for monosaccharification from corncobs. Biotechnol Biofuels 12:190PubMedPubMedCentralCrossRefGoogle Scholar
- Liu Y, Huang L, Zheng D et al (2019b) Biochemical characterization of a novel GH43 family beta-xylosidase from Bacillus pumilus. Food Chem 295:653–661PubMedCrossRefGoogle Scholar
- Long L, Zhao H, Ding D et al (2018) Heterologous expression of two Aspergillus niger feruloyl esterases in Trichoderma reesei for the production of ferulic acid from wheat. Bioprocess Biosyst Eng 41:593–601PubMedCrossRefGoogle Scholar
- Makela MR, Dilokpimol A, Koskela SM et al (2018) Characterization of a feruloyl esterase from Aspergillus terreus facilitates the division of fungal enzymes from carbohydrate esterase family 1 of the carbohydrate-active enzymes (CAZy) database. Microb Biotechnol 11:869–880PubMedPubMedCentralCrossRefGoogle Scholar
- Malgas S, Pletschke BI (2019) The effect of an oligosaccharide reducing-end xylanase, Bh Rex8A, on the synergistic degradation of xylan backbones by an optimised xylanolytic enzyme cocktail. Enzyme Microb Technol 122:74–81PubMedCrossRefGoogle Scholar
- Malgas S, Thoresen M, van Dyk SJ, Pletschke BI (2017) Time dependence of enzyme synergism during the degradation of model and natural lignocellulosic substrates. Enzyme Microb Technol 103:1–11PubMedCrossRefGoogle Scholar
- Martins MP, Ventorim RZ, Coura RR et al (2018) The beta-xylosidase from Ceratocystis fimbriata RM35 improves the saccharification of sugarcane bagasse. Biocatal Agric Biotechnol 13:291–298CrossRefGoogle Scholar
- McKee LS, Sunner H, Anasontzis GE et al (2016) A GH115 α-glucuronidase from Schizophyllum commune contributes to the synergistic enzymatic deconstruction of softwood glucuronoarabinoxylan. Biotechnol Biofuels 9:2PubMedPubMedCentralCrossRefGoogle Scholar
- Mendis M, Simsek S (2015) Production of structurally diverse wheat arabinoxylan hydrolyzates using combinations of xylanase and arabinofuranosidase. Carbohydr Polym 132:452–459PubMedCrossRefGoogle Scholar
- Moreira LRS, Filho EXF (2008) An overview of mannan structure and mannan-degrading enzyme systems. Appl Microbiol Biotechnol 79:165–178PubMedCrossRefGoogle Scholar
- Mosbech C, Holck J, Meyer AS, Agger JW (2018) The natural catalytic function of CuGE glucuronoyl esterase in hydrolysis of genuine lignin – carbohydrate complexes from birch. Biotechnol Biofuels 11:71PubMedPubMedCentralCrossRefGoogle Scholar
- Müller G, Várnai A, Johansen KS et al (2015) Harnessing the potential of LPMO-containing cellulase cocktails poses new demands on processing conditions. Biotechnol Biofuels 8:187PubMedPubMedCentralCrossRefGoogle Scholar
- Nagy T, Emami K, Fontes CMG et al (2002) The membrane-bound α-glucuronidase from Pseudomonas cellulosa hydrolyzes 4-O-methyl-D-glucuronoxylooligosaccharides but not 4-O- methyl-D-glucuronoxylan. J Biotechnol 184:4925–4929Google Scholar
- Nurizzo D, Nagy T, Gilbert HJ, Davies GJ (2002) The structural basis for catalysis and specificity of the Pseudomonas cellulosa alpha-glucuronidase, GlcA67A. Structure 10:547–556PubMedCrossRefGoogle Scholar
- Oliveira DM, Mota TR, Oliva B et al (2019) Feruloyl esterases : biocatalysts to overcome biomass recalcitrance and for the production of bioactive compounds. Bioresour Technol 278:408–423PubMedCrossRefGoogle Scholar
- Pinto PC, Evtuguin DV, Neto CP (2005) Structure of hardwood glucuronoxylans: modifications and impact on pulp retention during wood kraft pulping. Carbohydr Polym 60:489–497CrossRefGoogle Scholar
- Puchart V, Agger JW, Berrin J-G et al (2016) Comparison of fungal carbohydrate esterases of family CE16 on artificial and natural subtrates. J Biotechnol 233:228–236PubMedCrossRefGoogle Scholar
- Qing Q, Yang B, Wyman CE (2010) Xylooligomers are strong inhibitors of cellulose hydrolysis by enzymes. Bioresour Technol 101:9624–9630PubMedCrossRefGoogle Scholar
- Raweesri P, Riangrungrojana P, Pinphanichakarn P (2008) α-L-Arabinofuranosidase from Streptomyces sp. PC22: purification, characterization and its synergistic action with xylanolytic enzymes in the degradation of xylan and agricultural residues. Bioresour Technol 99:8981–8986PubMedCrossRefGoogle Scholar
- Rhee MS, Sawhney N, Kim YS et al (2017) GH115 α-glucuronidase and GH11 xylanase from Paenibacillus sp. JDR-2: potential roles in processing glucuronoxylans. Appl Microbiol Biotechnol 101:1465–1476PubMedCrossRefGoogle Scholar
- Rogowski A, Baslé A, Farinas CS et al (2014) Evidence that GH115 α-glucuronidase activity, which is required to degrade plant biomass, is dependent on conformational flexibility. J Biol Chem 289:53–64PubMedCrossRefGoogle Scholar
- Romano de Carvalho D, Carli S, Meleiro LP et al (2018) A halotolerant bifunctional beta-xylosidase/alpha-L-arabinofuranosidase from Colletotrichum graminicola: purification and biochemical characterization. Int J Biol Macromol 114:74–750Google Scholar
- Rosa L, Ravanal MC, Mardones W, Eyzaguirre J (2013) Characterization of a recombinant α-glucuronidase from Aspergillus fumigatus. Fungal Biol 117:380–387PubMedCrossRefGoogle Scholar
- Saha BC (2003) Hemicellulose bioconversion. J Ind Microbiol Biotechnol 30:279–291PubMedCrossRefGoogle Scholar
- Samanta AK, Jayapal N, Jayaram C et al (2015) Xylooligosaccharides as prebiotics from agricultural by-products : production and applications. Bioact Carbohydrates Diet Fibre 5:62–71CrossRefGoogle Scholar
- Sanhueza C, Carvajal G, Soto-aguilar J et al (2018) The effect of a lytic polysaccharide monooxygenase and a xylanase from Gloeophyllum trabeum on the enzymatic hydrolysis of lignocellulosic residues using a commercial cellulase. Enzyme Microb Technol 113:75–82PubMedCrossRefGoogle Scholar
- Santos CR, Hoffmam ZB, Peixoto V et al (2014) Molecular mechanisms associated with xylan degradation by Xanthomonas plant pathogens. J Biol Chem 289:32186–32200PubMedPubMedCentralCrossRefGoogle Scholar
- Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61:263–289PubMedCrossRefGoogle Scholar
- Schendel RR, Becker A, Tyl CE, Bunzel M (2015) Isolation and characterization of feruloylated arabinoxylan oligosaccharides from the perennial cereal grain intermediate wheat grass (Thinopyrum intermedium). Carbohydr Res 407:16–25PubMedCrossRefGoogle Scholar
- Sheng P, Xu J, Saccone G et al (2014) Discovery and characterization of endo-xylanase and beta-xylosidase from a highly xylanolytic bacterium in the hindgut of Holotrichia parallela larvae. J Mol Catal B 105:33–40CrossRefGoogle Scholar
- Shi P, Chen X, Meng K et al (2013) Distinct actions by Paenibacillus sp. strain E18 α-larabinofuranosidases and xylanase in xylan degradation. Appl Environ Microbiol 79:1990–1995PubMedPubMedCentralCrossRefGoogle Scholar
- Simmons TJ, Frandsen KEH, Ciano L et al (2017) Structural and electronic determinants of lytic polysaccharide monooxygenase reactivity on polysaccharide substrates. Nat Commun 8:1064PubMedPubMedCentralCrossRefGoogle Scholar
- Tenkanen M, Siika-Aho M (2000) An α-glucuronidase of Schizophyllum commune acting on polymeric xylan. J Biotechnol 78:149–161PubMedCrossRefGoogle Scholar
- Togashi H, Kato A, Shimizu K (2009) Enzymatically derived aldouronic acids from Eucalyptus globulus glucuronoxylan. Carbohydr Polym 78:247–252CrossRefGoogle Scholar
- Valenzuela SV, Lopez S, Biely P et al (2016) The glycoside hydrolase family 8 reducing-end xylose-releasing exo-oligoxylanase Rex8A from Paenibacillus barcinonensis BP-23 is active on branched xylooligosaccharides. Appl Environ Microbiol 82:5116–5124PubMedPubMedCentralCrossRefGoogle Scholar
- Van Dyk JS, Pletschke BI (2012) A review of lignocellulose bioconversion using enzymatic hydrolysis and synergistic cooperation between enzymes-Factors affecting enzymes, conversion and synergy. Biotechnol Adv 30:1458–1480PubMedCrossRefGoogle Scholar
- Wang L, Shi H, Xu B et al (2016) Characterization of Thermotoga thermarum DSM 5069 alpha-glucuronidase and synergistic degradation of xylan. BioResources 11:5767–5779Google Scholar
- Wefers D, Cavalcante JJV, Schendel RR et al (2017) Biochemical and structural analyses of two cryptic esterases in Bacteroides intestinalis and their synergistic activities with cognate xylanases. J Mol Biol 429:2509–2527PubMedCrossRefGoogle Scholar
- Westereng B, Cannella D, Agger JW et al (2015) Enzymatic cellulose oxidation is linked to lignin by long-range electron transfer. Sci Rep 5:18561PubMedPubMedCentralCrossRefGoogle Scholar
- Wong DWS, Chan VJ, Liao H, Zidwick MJ (2013) Cloning of a novel feruloyl esterase gene from rumen microbial metagenome and enzyme characterization in synergism with endoxylanases. J Ind Microbiol Biotechnol 40:287–295PubMedCrossRefGoogle Scholar
- Yan QJ, Wang L, Jiang ZQ et al (2008) A xylose-tolerant β-xylosidase from Paecilomyces thermophila: characterization and its co-action with the endogenous xylanase. Bioresour Technol 99:5402–5410PubMedCrossRefGoogle Scholar
- Yang C, Liu W (2008) Purification and properties of an acetylxylan esterase from Thermobifida fusca. Enzyme Microb Technol 42:181–186PubMedCrossRefGoogle Scholar
- Yang W, Bai Y, Yang P, et al. (2015) A novel bifunctional GH51 exo-α-L-arabinofuranosidase/endo-xylanase from Alicyclobacillus sp. A4 with significant biomass-degrading capacity. Biotechnol Biofuels 8: 197.PubMedPubMedCentralCrossRefGoogle Scholar
- Yang X, Shi P, Huang H et al (2014a) Two xylose-tolerant GH43 bifunctional β-xylosidase/α-arabinosidases and one GH11 xylanase from Humicola insolens and their synergy in the degradation of xylan. Food Chem 148:381–387PubMedCrossRefGoogle Scholar
- Yang X, Shi P, Ma R et al (2014b) A new GH43 alpha-arabinofuranosidase from Humicola insolens Y1: biochemical characterization and synergistic action with a xylanase on xylan degradation. Appl Biochem Biotechnol 175:1960–1970PubMedCrossRefGoogle Scholar
- Zhang J, Siika-Aho M, Tenkanen M, Viikari L (2011) The role of acetyl xylan esterase in the solubilization of xylan and enzymatic hydrolysis of wheat straw and giant reed. Biotechnol Biofuels 4:60PubMedPubMedCentralCrossRefGoogle Scholar
- Zheng F, Huang J, Yin Y (2013) A novel neutral xylanase with high SDS resistance from Volvariella volvacea: characterization and its synergistic hydrolysis of wheat bran with acetyl xylan esterase. J Ind Microbiol Biotechnol 40:1083–1093PubMedCrossRefGoogle Scholar
- Zhuo R, Yu H, Qin X et al (2018) Heterologous expression and characterization of a xylanase and xylosidase from white rot fungi and their application in synergistic hydrolysis of lignocellulose. Chemosphere 212:24–33PubMedCrossRefGoogle Scholar