Abstract
Xylan 1,4-β-D-xylosidase catalyzes hydrolysis of non-reducing end xylose residues from xylooligosaccharides. The enzyme is currently used in combination with β-xylanases in several large-scale processes for improving baking properties of bread dough, improving digestibility of animal feed, production of d-xylose for xylitol manufacture, and deinking of recycled paper. On a grander scale, the enzyme could find employment alongside cellulases and other hemicellulases in hydrolyzing lignocellulosic biomass so that reaction product monosaccharides can be fermented to biofuels such as ethanol and butanol. Catalytically efficient enzyme, performing under saccharification reactor conditions, is critical to the feasibility of enzymatic saccharification processes. This is particularly important for β-xylosidase which would catalyze breakage of more glycosidic bonds of hemicellulose than any other hemicellulase. In this paper, we review applications and properties of the enzyme with emphasis on the catalytically efficient β-d-xylosidase from Selenomonas ruminantium and its potential use in saccharification of lignocellulosic biomass for producing biofuels.
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Adelsberger H, Hertel C, Glawischnig E, Zverlov VV, Schwarz WH (2004) Enzyme system of Clostridium stercorarium for hydrolysis of arabinoxylan: reconstitution of the in vivo system from recombinant enzymes. Microbiology 150:2257–2266
Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201
Bourgois TM, Nguyen DV, Sansen S, Rombouts S, Beliën T, Fierens K, Raedschelders G, Rabijns A, Courtin CM, Delcour JA, Van Campenhout S, Volckaert G (2007) Targeted molecular engineering of a family 11 endoxylanase to decrease its sensitivity towards Triticum aestivum endoxylanase inhibitor types. J Biotechnol 130:95–105
Braun C, Meinke A, Ziser L, Withers SG (1993) Simultaneous high-performance liquid chromatographic determination of both the cleavage pattern and the stereochemical outcome of the hydrolysis reactions catalyzed by various glycosidases. Anal Biochem 212:259–262
Bravman T, Mechaly A, Shulami S, Belakhov V, Baasov T, Shoham G, Shoham Y (2001) Glutamic acid 160 is the acid-base catalyst of β-xylosidase from Bacillus stearothermophilus T-6: a family 39 glycoside hydrolase. FEBS Lett 495:115–119
Brunner PC, Keller N, McDonald BA (2009) Wheat domestication accelerated evolution and triggered positive selection in the β-xylosidase enzyme of Mycosphaerella graminicola. PLoS ONE 4:e7884
Brunzelle JS, Jordan DB, McCaslin DR, Olczak A, Wawrzak Z (2008) Structure of the two-subsite β-d-xylosidase from Selenomonas ruminantium in complex with 1,3-bis[tris(hydroxymethyl)methylamino]propane. Arch Biochem Biophys 474:157–166
Brüx C, Ben-David A, Shallom-Shezifi D, Leon M, Niefind K, Shoham G, Shoham Y, Schomburg D (2006) The structure of an inverting GH43 β-xylosidase from Geobacillus stearothermophilus with its substrate reveals the role of the three catalytic residues. J Mol Biol 359:97–109
Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37:D233–D238
Chen Y-L, Tang T-Y, Cheng K-J (2001) Directed evolution to produce an alkalophilic variant from Neocallimastix patriciarum xylanase. Can J Microbiol 47:1088–1094
Chundawat SPS, Balan V, Dale BE (2008) High-throughput microplate technique for enzymatic hydrolysis of lignocellulosic biomass. Biotechnol Bioeng 99:1281–1294
De Lemos Esteves F, Gouders T, Lamotte-Brasseur J, Rigali S, Frère J-M (2005) Improving the alkalophilic performances of the Xy11 xylanase from Streptomyces sp. S38: structural comparison and mutational analysis. Protein Sci 14:292–302
Dornez E, Gebruers K, Cuyvers S, Delcour JA, Courtin CM (2007) Impact of wheat flour-associated endoxylanases on arabinoxylan in dough after mixing and resting. J Agric Food Chem 55:7149–7155
Ducros VM, Tarling CA, Zechel DL, Brzozowski AM, Frandsen TP, von Ossowski I, Schülein M, Withers SG, Davies GJ (2003) Anatomy of glycosynthesis: structure and kinetics of the Humicola insolens Cel7B E197A and E197S glycosynthase mutants. Chem Biol 10:619–628
Durette PL, Horton D (1971) Conformational analysis of sugars and their derivatives. Adv Carbohydr Chem Biochem 26:49–125
Fan Z, Wagschal K, Lee CC, Kong Q, Shen KA, Maiti IB, Yuan L (2008) The construction and characterization of two xylan-degrading chimeric enzymes. Biotechnol Bioeng 102:684–692
Fan Z, Wagschal K, Chen W, Montross MD, Lee CC, Yuan L (2009a) Multimeric hemicellulases facilitate biomass conversion. Appl Environ Microbiol 75:1754–1757
Fan Z, Werkman JR, Yuan L (2009b) Engineering of a multifunctional hemicellulase. Biotechnol Lett 31:751–757
Fan Z, Yuan L, Jordan DB, Wagschal K, Heng C, Braker JD (2010) Engineering lower inhibitor affinities in β-D-xylosidase. Appl Microbiol Biotechnol. doi:10.1007/s00253-009-2335-7
Fenel F, Zitting A-J, Kantelinen A (2006) Increased alkali stability in Trichoderma reesei endo-1,4-β-xylanase II by site-directed mutagenesis. J Biotechnol 121:102–107
Fushinobu S, Hidaka M, Honda Y, Wakagi T, Shoun H, Kitaoka M (2005) Structural basis for the specificity of the reducing end xylose-releasing exo-oligoxylanase from Bacillus halodurans C-125. J Biol Chem 280:17180–17186
Gao D, Chundawat SPS, Krishnan C, Balan W, Dale BE (2010) Mixture optimization of six core glycosyl hydrolases for maximizing saccharification of ammonia fiber expansion (AFEX) pretreated corn stover. Bioresource Technol 101:2770–2781
Heinzelman P, Snow CD, Wu I, Nguyen C, Villalobos A, Govindarajan S, Minshull J, Arnold FH (2009) A family of thermostable fungal cellulases created by structure-guided recombination. Proc Nat Acad Sci 106:5610–5615
Honda Y, Kitaoka M (2004) A family 8 glycoside hydrolase from Bacillus halodurans C-125 (BH2105) is a reducing end xylose-releasing exo-oligoxylanase. J Biol Chem 279:55097–55103
Jordan DB (2008) β-d-Xylosidase from Selenomonas ruminantium: catalyzed reactions with natural and artificial substrates. Appl Biochem Biotechnol 146:137–149
Jordan DB, Braker JD (2007) Inhibition of the two-subsite β-d-xylosidase from Selenomonas ruminantium by sugars: competitive, noncompetitive, double binding, and slow binding modes. Arch Biochem Biophys 465:231–246
Jordan DB, Braker JD (2009) β-d-Xylosidase from Selenomonas ruminantium: thermodynamics of enzyme-catalyzed and noncatalyzed reactions. Appl Biochem Biotechnol 155:330–346
Jordan DB, Braker JD (2010) β-d-Xylosidase from Selenomonas ruminantium: role of glutamate 186 in catalysis revealed by site-directed mutagenesis, alternate substrates, and active-site inhibitor. Appl Biochem Biotechnol 161:395–410. doi:10.1007/s12010-009-8874-7
Jordan DB, Li X-L (2007) Variation in relative substrate specificity of bifunctional β-d-xylosidase/α-l-arabinofuranosidase by single-site mutations: roles of substrate distortion and recognition. Biochim Biophys Acta 1774:1192–1198
Jordan DB, Li X-L, Dunlap CA, Whitehead TR, Cotta MA (2007a) β-d-Xylosidase from Selenomonas ruminantium of glycoside hydrolase family 43. Appl Biochem Biotechnol 136–140:93–104
Jordan DB, Li X-L, Dunlap CA, Whitehead TR, Cotta MA (2007b) Structure–function relationships of a catalytically efficient β-d-xylosidase. Appl Biochem Biotechnol 141:51–76
Jordan DB, Mertens JA, Braker JD (2009) Aminoalcohols as probes of the two-subsite active site of β-d-xylosidase from Selenomonas ruminantium. Biochim Biophys Acta 1794:144–158
Kersters-Hilderson H, Claeyssens M, Doorslaer EV, De Bruyne CK (1976) Determination of the anomeric configuration of d-xylose with d-xylose isomerases. Carbohydr Res 140:342–346
Kim YW, Chen H, Withers SG (2005) Enzymatic transglycosylation of xylose using a glycosynthase. Carbohydr Res 340:2735–2741
Klinke HB, Thomsen AB, Ahring BK (2004) Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl Microbiol Biotechnol 66:10–26
Konstantinidis AK, Marsden I, Sinnott ML (1993) Hydrolyses of α- and β-cellobiosyl fluorides by cellobiohydrolases of Trichoderma reesei. Biochem J 291:883–888
Koshland DE (1953) Stereochemistry and mechanism of enzyme reactions. Biol Rev 28:416–436
La Grange DC, Pretorius IS, Claeyssens M, van Zyl WH (2001) Degradation of xylan to d-xylose by recombinant Saccharomyces cerevisiae coexpressing the Aspergillus niger β-xylosidase (xlnD) and the Trichoderma reesei xylanase II (xyn2) genes. Appl Environ Microbiol 67:5512–5519
Larsson S, Palmqvist E, Hahn-Hägerdal B, Tengborg C, Stenberg K, Zacchi G, Nilvebrant NO (1999) The generation of fermentation inhibitors during dilute acid hydrolysis of softwood. Enzyme Microb Technol 24:151–159
Lairson LL, Withers SG (2004) Mechanistic analogies amongst carbohydrate modifying enzymes. Chem Commun 2:2243–2248
Lebbink JHG, Kaper T, Bron P, van der Oost J, de Vos WM (2000) Improving low-temperature catalysis in the hyperthermostable Pyrococcus furiosus β-glucosidase CelB by directed evolution. Biochemistry 39:3656–3665
Lin L, Meng X, Liu P, Hong Y, Wu G, Huang X, Li C, Dong J, Xiao L, Liu Z (2009) Improved catalytic efficiency of endo-β-1,4-glucanase from Bacillus subtilis BME-15 by directed evolution. Appl Microbiol Biotechnol 82:671–679
Liu L, Wang B, Chen H, Wang S, Wang M, Zhang S, Song A, Shen J, Wu K, Jia X (2009) Rational pH-engineering of the thermostable xylanase based on computational model. Process Biochem 44:912–915
Lopez-Camacho C, Salgado J, Lequerica JL, Madarro A, Ballestar E, Franco L, Polaina J (1996) Amino acid substitutions enhancing the thermostability of Bacillus polymyxa β-glucosidase A. Biochem J 314:833–838
Lovering AL, Lee SS, Kim Y-W, Withers SG, Strynadka NCJ (2005) Mechanistic and structural analysis of a family 31 α-glycosidase and its glycosyl-enzyme intermediate. J Biol Chem 280:2105–2115
Luo CD, Brink DL, Blanch HW (2002) Identification of potential fermentation inhibitors in conversion of hybrid poplar hydrolyzate to ethanol. Biomass Bioenergy 22:125–138
Manzanares P, Ramon D, Querol A (1999) Screening of non-Saccharomyces wine yeasts for production of β-xylosidase activity. Int J Food Micro 46:105–112
Marques S, Pala H, Alves L, Amaral-Collaço MT, Gama FM, Gírio FM (2003) Characterisation and application of glycanases secreted by Aspergillus terreus CCMI 498 and Trichoderma viride CCMI 84 for enzymatic deinking of mixed office wastepaper. J Biotechnol 100:209–219
Okuyama M, Kaneko A, Mori H, Chiba S, Kimura A (2006) Structural elements to convert Escherichia coli α-xylosidase (YicI) into α-glucosidase. FEBS Lett 580:2707–2711
Palmqvist E, Almeida JS, Hahn-Hägerdal B (1999) Influence of furfural on anaerobic glycolytic kinetics of Saccharomyces cerevisiae in batch culture. Biotechnol Bioeng 62:447–454
Polizeli MLTM, Rizzatti ACS, Monti R, Terenzi HF, Jorge JA, Amorim DS (2005) Xylanases from fungi: properties and industrial applications. Appl Microbiol Biotechnol 67:577–591
Rasmussen LE, Sørensen HR, Vind J, Viksø-Nielsen A (2006) Mode of action and properties of the β-xylosidases from Talaromyces emersonii and Trichoderma reesi. Biotechnol Bioengineer 94:869–876
Rempel BP, Withers SG (2008) Covalent inhibitors of glycosidases and their applications in biochemistry and biology. Glycobiology 18:570–586
Rye CS, Withers SG (2000) Glycosidase mechanisms. Curr Opin Chem Biol 4:573–580
Shaikh FA, Withers SG (2008) Teaching old enzymes new tricks: engineering and evolution of glycosidases and glycosyl transferases for improved glycoside synthesis. Biochem Cell Biol 86:169–177
Shallom D, Leon M, Bravman T, Ben-David A, Zaide G, Belakhov V, Shoham G, Schomburg D, Baasov T, Shoham Y (2005) Biochemical characterization and identification of the catalytic residues of a family 43 β-d-xylosidase from Geobacillus stearothermophilus T-6. Biochemistry 44:387–397
Sinnott ML (2007) Carbohydrate chemistry and biochemistry. Structure and mechanism. The Royal Society of Chemistry, Cambridge
Sørensen HR, Pedersen S, Jørgensen CT, Meyer AS (2007) Enzymatic hydrolysis of wheat arabinoxylan by a recombinant “minimal” enzyme cocktail containing β-xylosidase and novel endo-1,4-β-xylanase and α-l-arabinofuranosidase activities. Biotechnol Prog 23:100–107
Smaali I, Rémond C, O’Donohue MJ (2006) Expression in Escherichia coli and characterization of β-xylosidases GH39 and GH-43 from Bacillus halodurans C-125. Appl Microbiol Biotechnol 73:582–590
Taylor LE, Dai Z, Decker SR, Brunecky R, Adney WS, Ding S-Y, Himmel ME (2008) Heterologous expression of glycosyl hydrolases in planta: a new departure for biofuels. Trends in Biotechnol 26:413–424
Tsujibo H, Takada A, Kosaka M, Miyamoto K, Inamori Y (2001) Cloning, sequencing, and expression of the gene encoding an intracellular β-d-xylosidase from Streptomyces thermoviolaceus OPC-520. Biosci Biotech Biochem 65:1824–1831
Umemoto Y, Onishi R, Araki T (2008) Cloning of a novel gene encoding β-1,3-xylosidase from a marine bacterium, Vibrio sp. strain XY-214, and characterization of the gene product. Appl Environ Microbiol 74:305–308
Umemoto H, Ihsanawati IM, Yatsunami R, Fukui T, Kumasaka T, Tanaka N, Nakamura S (2009) Improvement of alkaliphily of Bacillus alkaline xylanase by introducing amino acid substitutions both on catalytic cleft and protein surface. Biosci Biotechnol Biochem 73:965–967
Van Doorslaer E, Kersters-Hilderson H, De Bruyne CK (1985) Hydrolysis of β-d-xylo-oligosaccharides by β-d-xylosidase from Bacillus pumilus. Carbohydr Res 140:342–346
Vocadlo DJ, Mackenzie LF, He S, Zeikus GJ, Withers SG (1998) Identification of Glu-277 as the catalytic nucleophile of Thermoanaerobacterium saccharolyticum β-xylosidase using electrospray MS. Biochem J 335:449–455
Wagschal K, Franqui-Espiet D, Lee CC, Robertson GH, Wong DW (2005) Enzyme-coupled assay for β-xylosidase hydrolysis of natural substrates. Appl Environ Microbiol 71:5318–5323
Wagschal K, Franqui-Espiet C, Lee CC, Kibblewhite-Accinelli RE, Robertson GH, Wong DW (2007) Genetic and biochemical characterization of an α-l-arabinofuranosidase isolated from a compost starter mixture. Enz Microbial Technol 40:747–753
Wagschal K, Franqui-Espiet D, Lee CC, Robertson GH, Wong DW (2008) Cloning, expression and characterization of a glycoside hydrolase family 39 xylosidase from Bacillus halodurans C-125. Appl Biochem Biotechnol 146:69–78
Wagschal K, Heng C, Lee CC, Robertson GH, Orts WJ, Wong DW (2009a) Purification and characterization of a glycoside hydrolase family 43 β-xylosidase from Geobacillus thermoleovorans IT-08. Appl Biochem Biotech 155:304–313
Wagschal K, Heng C, Lee CC, Wong DW (2009b) Biochemical characterization of a novel dual-function arabinofuranosidase/xylosidase isolated from a compost starter mixture. Appl Microbiol Biotechnol 81:855–863
Wen F, Nair NU, Zhao H (2009) Protein engineering in designing tailored enzymes and microorganisms for biofuels production. Curr Opin Biotechnol 20:412–419
Werpy T, Petersen G (2004) Top value added chemicals from biomass, volume 1-results of screening for potential candidates from sugars and synthesis gas. US Department of Energy, Washington. DC. http://www.pnl.gov/main/publications/external/technicalreports/PNNL-14808.pdf
Williams JS, Hoos R, Withers SG (2000) Nanomolar versus millimolar inhibition by xylobiose-derived azasugars: significant differences between two structurally distinct xylanases. J Am Chem Soc 122:2223–2234
Withers SG (2001) Enzymatic cleavage of glycosides: how does it happen? Pure Appl Chem 67:1673–1682
Wong DWS, Batt SB, Lee CC, Robertson GH (2003) Direct screening of libraries of yeast clones for α-amylase activity on raw starch hydrolysis. Protein Pept Lett 10:459–468
Wong DWS, Batt SB, Lee CC, Robertson GH (2004) High-activity barley α-amylase by directed evolution. Protein J 23:453–460
Xiao Z, Zhang X, Gregg DJ, Saddler JN (2004) Effects of sugar inhibition on cellulases and β-glucosidase during enzymatic hydrolysis of softwood substrates. Appl Microbiol Biotechnol 115:1115–1126
Xu W-W, Shima Y, Negoro S, Urabe I (1991) Sequence and properties of β-xylosidase from Bacillus pumilus IPO. Contradiction of the previous nucleotide sequence. Eur J Biochem 202:1197–1203
Yamaguchi T, Matsumoto Y, Shirakawa M, Kibe M, Hibino T, Kozaki S, Takasaki Y, Nitta Y (1996) Cloning, sequencing, and expression of a β-amylase gene from Bacillus cereus var. mycoides and characterization of its products. Biosci Biotechnol Biochem 60:1255–1259
Yip VL, Withers SG (2006) Breakdown of oligosaccharides by the process of elimination. Curr Opin Chem Biol 10:147–155
Yoshikawa K, Yamamoto K, Okada S (1994) Transfer action of α-d-xylosidases from Aspergillus flavus MO-5 on p-nitrophenyl-α-d-xylopyranoside. Biosci Biotechnol Biochem 58:121–125
Yuan L, Kurek I, English J, Keenan R (2005) Laboratory-directed protein evolution. Microbiol Mol Biol Rev 69:373–392
Zanoelo FF, Polizeli MLTM, Terenzi HF, Jorge JA (2004) Purification and biochemical properties of a thermostable xylose-tolerant β-d-xylosidase from Scytalidium thermophilum. J Ind Microbiol Biotech 31:170–176
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This work was supported by United States Department of Agriculture CRIS 5325-41000-046-00 (K.W.) and CRIS 3620-41000-118-00D (D.B.J.). The mention of firm names or trade products does not imply that they are endorsed or recommended by the US Department of Agriculture over other firms or similar products not mentioned.
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Jordan, D.B., Wagschal, K. Properties and applications of microbial β-D-xylosidases featuring the catalytically efficient enzyme from Selenomonas ruminantium . Appl Microbiol Biotechnol 86, 1647–1658 (2010). https://doi.org/10.1007/s00253-010-2538-y
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DOI: https://doi.org/10.1007/s00253-010-2538-y