Abstract
Industrial applications of xylanases have made this enzyme an important subject of applied research work. Function of this particular enzyme is to degrade or hydrolyze the plentiful polysaccharide xylan, an important component of hemicellulose. It mainly cleaves the backbone of xylan that is made up of a number of xylose residues connected with β-1,4-glycosidic linkages. Fungi with mycelia are regarded as the best producer of xylanases. These varied xylanases not only differ in their sizes and shapes but also differ in their physicochemical properties. Depending on the optimum pH in which they work best, they have been classified into (1) acidophilic xylanases active at low pH or acidic pH range, (2) alkaliphilic xylanases that are active at high or alkaline pH range and (3) neutral xylanases having pH optima in the neutral range between pH 5 and 7. Other researchers have classified the xylanases also on the basis of their structural properties, kinetic parameters, etc. This review discusses the molecular structures of some acidophilic xylanases and the molecular basis of low pH optima observed for their activities. It also discusses their unique catalytic mechanism and actual role of the catalytic residues found in them. Apart from these, the review also discusses different applications of these acidophilic xylanases in different industries. The article concludes with brief suggestions about how these acidophilic xylanases can be created employing the techniques of genetic engineering and concepts of synthetic evolution, using the traits of the known acidophilic xylanases discussed in the review.
Similar content being viewed by others
References
Al Balaa B, Wouters J, Dogne S, Rossini C, Schaus JM, Depiereux E, Vandenhaute J, Housen I (2006) Identification, cloning, and expression of the Scytalidium acidophilum XYL1 gene encoding for an acidophilic xylanase. Biosci Biotechnol Biochem 70:269–272
Alvira P, Tomás-Pejó E, Ballesteros M, Negro MJ (2010) Pretreatment technologies for an efficient bioethanol production process based on enzymatic hydrolysis: a review. Bioresour Technol 101:4851–4861
Bayer EA, Chanzy H, Lamed R, Shoham Y (1998) Cellulose, cellulases and cellulosomes. Curr Opin Struct Biol 8:548–557
Beg QK, Kapoor M, Mahajan L, Hoondal GS (2001) Microbial xylanases and their industrial applications: a review. Appl Microbiol Biotechnol 56:326–338
Belancic A, Scarpa J, Peirano A, Diaz R, Steiner J, Eyzaguirre J (1995) Penicillium purpurogenum produces several xylanases: purification and properties of two of the enzymes. J Biotechnol 41:71–79
Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig Shindyalov HIN, Bourne PE (2000) The protein data bank. Nucl Acids Res 28:235–242
Berrin JG, Williamson G, Puigserver A, Chaix JC, McLauchlan WR, Juge N (2000) High-level production of recombinant fungal endo-β-1,4-xylanase in the methylotrophic yeast Pichia pastoris. Protein Expr Purif 19:179–187
Biely P (1985) Microbial xylanolytic systems. Trends Biotechnol 3:286–290
Biely P, Vrsanská M, Krátký Z (1981) Mechanisms of substrate digestion by endo-1,4-beta-xylanase of Cryptococcus albidus. Lysozyme-type pattern of action. Eur J Biochem 119:565–571
Biely P, Vrsanská M, Tenkanen M, Kluepfel D (1997) Endo-beta-1,4-xylanase families: differences in catalytic properties. J Biotechnol 57:151–166
Biely P, Singh S, Puchart V (2016) Towards enzymatic breakdown of complex plant xylan structures: state of the art. Biotechnol Adv 34:1260–1274
Cao YH, Qiao JY, Li YH, Lu WQ (2007) De novo synthesis, constitutive expression of Aspergillus sulphureus β-xylanase gene in Pichia pastoris and partial enzymic characterization. Appl Microbiol Biotechnol 76:579–585
Carmona EC, Brochetto-Braga MR, Pizzirani-Kleiner AA, Jorge JA (1998) Purification and biochemical characterization of an endoxylanase from Aspergillus versicolor. FEMS Microbiol Lett 166:311–315
Chen Q, Li M, Wang X (2016) Enzymology properties of two different xylanases and their impacts on growth performance and intestinal microflora of weaned piglets. Anim Nutr 2:18–23
Claassen PAM, van Lier JB, Contreras AML, van Niel EWJ, Sijtsma L, Stams AJM, de Vries SS, Weusthuis RA (1999) Utilisation of biomass for the supply of energy carriers. Appl Microbiol Biotechnol 52:741–755
Collins T, Gerday C, Feller G (2005) Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol Rev 29:3–23
Correia MAS, Mazumder K, Brás JLA, Firbank SJ, Zhu Y, Lewis RJ, York WS, Fontes CMGA, Gilbert HJ (2011) Structure and function of an arabinoxylan-specific xylanase. J Biol Chem 286:22510–22520
Coughlan GP, Hazlewood MP (1993) β-1,4-d-xylan-degrading enzyme system: biochemistry, molecular biology, and applications. Biotechnol Appl Biochem 17:259–289
Coutinho PM, Henrissat B (1999) Carbohydrate-active enzyme server (CAZY). http://afmb.cnrs-mrs.fr/~cazy/CAZY/
Davies G, Henrissat B (1995) Structures and mechanisms of glycosyl hydrolases. Structure 3:853–859
Driss D, Bhiri B, Elleuch L, Bouly N, Stals I, Miled N, Blibech M, Ghorbel R, Chaaboun SE (2011) Purification and properties of an extracellular acidophilic endo-1,4-β-xylanase, naturally deleted in the “thumb”, from Penicillium occitanis Pol6. Process Biochem 46:1299–1306
Ebringerova A, Heinze T (2000) Xylan and xylan derivatives— biopolymers with valuable properties. 1. Naturally occurring xylans structures, isolation procedures and properties. Macromol Rapid Commun 21:542–556
Enshasy HAE, Kandiyli SK, Malek R, Othman NZ (2016) Microbial xylanases: sources, types and their application. In: Gupta VK (EDS) Microbial enzymes in bioconversions of biomass, Chap 7. Springer, Switzerland, pp 151–214
Fushinobu S, Ito K, Konno M, Wakagi T, Matsujawa H (1998) Crystalographic and mutational analyses of an extremely acidophilic and acid-stable xylanase: biased distribution of acidic residues and importance of Asp37 for catalysis at low pH. Protein Eng 11:1121–1128
Fushinobu S, Uno T, Kitaoka M, Hayashi K, Matsuzawa H, Wakagi T (2011) Mutational analysis of fungal family 11 xylanases on pH optimum determination. J Appl Glycos 58:107–114
Galbe M, Zacchi G (2002) A review of the production of ethanol from softwood. Appl Microbiol Biotechnol 59:618–628
Galbe M, Zacchi G (2007) Pretreatment of lignocellulosic materials for efficient bioethanol production. Adv Biochem Eng Biotechnol 108:41–65
Goldman SL, Kole C (2014) Compendium of bioenergy plants: Corn. CRC press Taylor and Francis group
Golugiri BR, Thulluri C, Cherupally M, Nidadavolu N, Achuthananda D, Mangamuri LN, Addepally U (2012) Potential of thermo and alkali stable xylanases from Thielaviopsis basicola (MTCC- 1467) in biobleaching of wood Kraft pulp. Appl Biochem Biotechnol 167:2369–2380
Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, Lopez R (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucl Acids Res 38(Suppl):W695–W699. https://doi.org/10.1093/nar/gkq313
Henrissat B, Bairoch A (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 293:781–788
Henrissat B, Coutinho PM (2001) Classification of glycoside hydrolases and glycosyltransferases from hyperthermophiles. Methods Enzymol 330:183–201
Henrissat B, Claeyssens M, Tomme P, Lemesle L, Mornon JP (1989) Cellulase families revealed by hydrophobic cluster analysis. Gene 81:83–95
Hessing JGM, van Rotterdam C, Verbakel JMA, Roza M, Maat J, van Gorcom RFM, van den Hondel CAMJJ (1994) Isolation and characterization of a 1,4-β-endoxylanase gene of A. awamori. Curr Genet 26:228–232
Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315:804–807
Iefuji H, Chino M, Kato M, Iimura Y (1996) Acid xylanase from yeast Cryptococcus sp. S-2: purification, characterization, cloning, and sequencing. Biosci Biotech Biochem 60:1331–1338
Jeffries TW (1996) Biochemistry and genetics of microbial xylanases. Curr Opin Biotechnol 7:337–342
Juturu V, Wu JC (2011) Microbial xylanases: engineering, production and industrial applications. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2011.11.006
Kimura T, Ito J, Kawano A, Makino T, Kondo H, Karita S, Sakka K, Ohmiya K (2000) Purification, characterization, and molecular cloning of acidophilic xylanase from Penicillium sp. 40. Biosci Biotechnol Biochem 64:1230–1237
Kittelmann S, Janssen PH (2011) Characterization of rumen ciliate community composition in domestic sheep, deer, and cattle, feeding on varying diets, by means of PCR-DGGE and clone libraries. FEMS Microbiol Ecol 75:468–481
Knob A, Carmona EC (2010) Purification and characterization of two extracellular xylanases from Penicillium sclerotiorum: a novel acidophilic xylanase. Appl Biochem Biotechnol 162:429–443
Knob A, Beite SM, Fortkamp D, Terrasan CRF, Almeida AFD (2013) Production, purification and characterization of a major Penicillium glabrum xylanase using brewer’s spent grain as substrate. Biomed Res Int 2013:728–735
Korona B, Korona D, Bielecki S (2006) Efficient expression and secretion of two co-produced xylanases from Aspergillus niger in Pichia pastoris directed by their native signal peptides and the Saccharomyces cerevisiae alpha-mating factor. Enzyme Microb Technol 39:683–689
Krengel U, Dijkstra BW (1996) Three-dimensional structure of endo-1,4-b-xylanase I from Aspergillus niger: molecular basis for its low pH optimum. J Mol Biol 263:70–78
Kuhad RC, Singh A (1993) Lignocellulose biotechnology: current and future prospects. Crit Rev Biotechnol 13:151–172
Kuhad RC, Singh A, Eriksson KE (1997) Microorganisms and enzymes involved in the degradation of plant fiber cell walls. Adv Biochem Eng Biotechnol 57:45–125
Liao H, Zheng H, Li S, Wei Z, Mei X, Ma H, Shen Q, Xu Y (2015) Functional diversity and properties of multiple xylanases from Penicillium oxalicum GZ-2. Sci Rep 5:12631
Ljungdahl LG (2008) The cellulase/hemicellulase system of the anaerobic fungus Orpinomyces PC-2 and aspects of its applied use. Ann NY Acad Sci 1125:308–321
Luo HY, Wang Y, Li J, Wang H, Yang J, Yang YH, Huang H, Fan Y, Yao B (2009) Cloning, expression and characterization of a novel acidic xylanase, XYL11B, from the acidophilic fungus Bispora sp. MEY-1. Enzyme Microb Technol 45:126–133
McCarter JD, Withers SG (1994) Mechanisms of enzymatic glycoside hydrolysis. Curr Opin Struct Biol 4:885–892
McWilliam H, Li W, Uludag M, Squizzato S, Park YM, Buso N, Cowley AP, Lopez R (2013) Analysis tool web services from the EMBL-EBI. Nucl Acids Res 41:W597–W600
Michaux C, Pouyez J, Mayard A, Vandurm P, Housen I, Wouters J (2010) Structural insights into the acidophilic pH adaptation of a novel endo-1,4-beta-xylanase from Scytalidium acidophilum. Biochimie 92:1407–1415
Motta FL, Andrade CCP, Santana MHA (2013) Review of xylanase production by the fermentation of xylan: classification, characterization and applications. In: Chandel AK, Silva SSd (eds) Sustainable degradation of lignocellulosic biomass—techniques, applications and commercialization. InTech http://dx.doi.org/10.5772/53544
Moore MM (2009) Genetic engineering of fungal cells. In: Doelle HW, Rokem S (eds) Biotechnology, Fundamentals in Biotechnology, Encyclopedia of life support systems (EoLSS) vol. 3, pp.36–66
Mukherjee M, Sengupta S (1985) An inducible xylanase of the mushroom Termitomyces clypeatus differing from the xylanase/amylase produced in dextrin medium. J Gen Microbiol 131:1881–1885
Ohta K, Moriyama S, Tanaka H, Shige T, Akimoto H (2001) Purification and characterization of an acidophilic xylanase from Aureobasidium pullulans var. melanigenum and sequence analysis of the encoding gene. J Biosci Bioeng 92:262–270
Paes G, Berrin JG, Beaugrand J (2012) GH11 xylanases: structure/function/properties relationships and applications. Biotechnol Adv 30:564–592
Parachin NS, Siqueira S, deFaria FP, Torres FAG, deMoraes LMP (2009) Xylanases from Cryptococcus flavus isolate I-11: enzymatic profile, isolation and heterologous expression of CfXYN1 in Saccharomyces cerevisiae. J Mol Catal B Enzym 59:52–57
Pokhrel S, Joo JC, Yoo YJ (2013) Shifting the Optimum pH of Bacillus circulans xylanase towards acidic side by introducing arginine. Biotechnol Bioproc E 18:35–42
Polizeli LTM, Rizzatti ACS, Monti R, Terenzi HF, Jorge JA, Amorim DS (2005) Xylanases from fungi: properties and industrial applications. Appl Microbiol Biotechnol 67:577–591
Ruller R, Alponti J, Deliberto LA, Ward RJ (2014) Concomitant adaptation of GH11 xylanase by directed evolution to create an alkali tolerant/thermophilic enzyme. Protein Eng Des Sel 27:255–262
Rye CS, Withers SG (2000) Glycosidase mechanisms. Curr Opin Chem Biol 4:573–580
Sanchez C (2008) Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol Adv 27:185–194
Sapag A, Wouters J, Lambert C, de Ioannes P, Eyzaguirre J, Depiereux E (2002) The endoxylanases from family 11: computer analysis of protein sequences reveals important structural and phylogenetic relationships. J Biotechnol 95:109–131
Schell DJ, Farmer J, Newman M, McMillan JD (2003) Dilute-sulfuric acid pretreatment of corn stover in pilot-scale reactor: investigation of yields, kinetics, and enzymatic digestibilities of solids. Appl Biochem Biotechnol 105:69–85
Schulze E (1891) Information regarding chemical composition of plant cell membrane. Ber Dtsch Chem Ges 24:2277–2287
Sharma A, Parashar D, Satyanarayana T (2016) Acidophilic microbes: biology and applications. In: Rampelotto PH (ed) Biotechnology of extremophiles: advances and challenges, Chap 7. Switzerland: Springer, 215–242
Sievers F, Wilm A, Dineen DG, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins D (2011) Fast scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Sys Biol 7:539
Singh S, Madlala AM, Prior BA (2003) Thermomyces lanuginosus: properties of strains and their hemicellulases. FEMS Microbiol Rev 27:3–16
Sunna A, Antranikian G (1997) Xylanolytic enzymes from fungi and bacteria. Crit Rev Biotechnol 17:39–67
Tenkanen M, Viikari L, Buchert J (1997) Use of acid-tolerant xylanase for bleaching of kraft pulps. Biotechnol Tech 11:935–993
Tomás-Pejó E, Oliva JM, Ballesteros M (2008) Realistic approach for full-scale bioethanol production from lignocellulose: a review. J Sci Ind Res 67:874–884
Törrönen A, Rouvinen J (1995) Structural comparison of two major endo-1,4-xylanases from Trichoderma reesei. Biochemistry 34:847–856
Törrönen A, Harkki A, Rouvinen J (1994) Three-dimensional structure of endo-1,4-β-xylanase II from Trichoderma reesei: two conformational states in the active site. EMBO J 13:2493–2501
Uffen RL (1997) Xylan degradation: a glimpse at microbial diversity. J Ind Microbiol Biotechnol 19:1–6
van den Broeck HC, de Graaff LH, Hille JDR, van Ooyen AJ, Visser J, Harder A (1992) Cloning and expression of xylanase genes from fungal origin. European Patent Application EPA 0463706A1, Gist-Brocades, Delft
Verma D, Satyanarayana T (2012) Molecular approaches for ameliorating microbial xylanases. Bioresour Technol 17:360–367
Viikari L, Kantelinen A, Sundquist J, Linko M (1994) Xylanases in bleaching, from an idea to the industry. FEMS Microbiol Rev 13:335–350
Voragen AGJ, Gruppen H, Verbruggen MA, Vietor RJ (1992) Characterization of cereals arabinoxylans. In: Visser J et al. (eds) Xylan and xylanases, vol 7. Elsevier Amsterdam, pp 51–67
VršanskáIlona M, Gorbacheva IV, Krátký Z, Biely P (1982) Reaction pathways of substrate degradation by an acidic endo-1,4-β-xylanase of Aspergillus niger. Biochim Biophys Acta Protein Struct Mol Enzymol 704:114–122
Wakarchuk WW, Campbell RL, Sung WL, Davodi J, Yaguchi M (1994) Mutational and crystallographic analyses of the active site residues of the Bacillus circulans xylanase. Protein Sci 3:467–475
Weng JK, Li X, Bonawitz ND, Chapple C (2008) Emerging strategies of lignin engineering and degradation for cellulosic biofuel production. Curr Opin Biotechnol 19:166–172
Whistler RL, Richards EL (1970) Hemicelluloses. In: Pigman W, Horton D (eds) The carbohydrates. Academic, pp 447–469
Wong KK, Tan LU, Saddler JN (1988) Multiplicity of β-1,4-xylanase in microorganisms: functions and applications. Microbiol Rev 52:305–317
Yang W, Yang Y, Zhang L, Xu H, Guo X, Yang X, Dong B, Cao Y (2017) Improved thermostabilty of an acidic xylanase from Aspergillus sulphureus by combined disulphide bridge introduction and proline residue substitution. Sci Rep 7:1587
Yi XL, Shi Y, Xu H, Li W, Xie J, Yu RQ, Zhu J, Cao Y, Qiao D (2010) Hyperexpression of two Aspergillus niger xylanase genes in Escherichia coli and characterization of the gene products. Braz J Microbiol 41:778–786
Zechel DL, Withers SG (2000) Glycosidase mechanisms: anatomy of a finely tuned catalyst. Acc Chem Res 33:11–18
Zhu H, Paradis FW, Krell PJ, Phillips JP, Forsberg CW (1994) Enzymatic specificities and modes of action of the two catalytic domains of the XynC xylanase from Fibrobacter succinogenes S85. J Bacteriol 176:3885–3894
Acknowledgements
PD is thankful to the University Grant Commission, India and Visva-Bharati University for financial assistance.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
There is no conflict of interest between any of the author.
Ethical statement
This article does not contain any studies with human participants or animals performed by any of the authors.
Rights and permissions
About this article
Cite this article
Dey, P., Roy, A. Molecular structure and catalytic mechanism of fungal family G acidophilic xylanases. 3 Biotech 8, 78 (2018). https://doi.org/10.1007/s13205-018-1091-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-018-1091-8