Skip to main content
Log in

Molecular structure and catalytic mechanism of fungal family G acidophilic xylanases

  • Review Article
  • Published:
3 Biotech Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bayer EA, Chanzy H, Lamed R, Shoham Y (1998) Cellulose, cellulases and cellulosomes. Curr Opin Struct Biol 8:548–557

    Article  CAS  Google Scholar 

  • Beg QK, Kapoor M, Mahajan L, Hoondal GS (2001) Microbial xylanases and their industrial applications: a review. Appl Microbiol Biotechnol 56:326–338

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Biely P (1985) Microbial xylanolytic systems. Trends Biotechnol 3:286–290

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Biely P, Vrsanská M, Tenkanen M, Kluepfel D (1997) Endo-beta-1,4-xylanase families: differences in catalytic properties. J Biotechnol 57:151–166

    Article  CAS  Google Scholar 

  • Biely P, Singh S, Puchart V (2016) Towards enzymatic breakdown of complex plant xylan structures: state of the art. Biotechnol Adv 34:1260–1274

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Collins T, Gerday C, Feller G (2005) Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol Rev 29:3–23

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Coughlan GP, Hazlewood MP (1993) β-1,4-d-xylan-degrading enzyme system: biochemistry, molecular biology, and applications. Biotechnol Appl Biochem 17:259–289

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Galbe M, Zacchi G (2002) A review of the production of ethanol from softwood. Appl Microbiol Biotechnol 59:618–628

    Article  CAS  Google Scholar 

  • Galbe M, Zacchi G (2007) Pretreatment of lignocellulosic materials for efficient bioethanol production. Adv Biochem Eng Biotechnol 108:41–65

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Henrissat B, Bairoch A (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 293:781–788

    Article  CAS  Google Scholar 

  • Henrissat B, Coutinho PM (2001) Classification of glycoside hydrolases and glycosyltransferases from hyperthermophiles. Methods Enzymol 330:183–201

    Article  CAS  Google Scholar 

  • Henrissat B, Claeyssens M, Tomme P, Lemesle L, Mornon JP (1989) Cellulase families revealed by hydrophobic cluster analysis. Gene 81:83–95

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jeffries TW (1996) Biochemistry and genetics of microbial xylanases. Curr Opin Biotechnol 7:337–342

    Article  CAS  Google Scholar 

  • Juturu V, Wu JC (2011) Microbial xylanases: engineering, production and industrial applications. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2011.11.006

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kuhad RC, Singh A (1993) Lignocellulose biotechnology: current and future prospects. Crit Rev Biotechnol 13:151–172

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • McCarter JD, Withers SG (1994) Mechanisms of enzymatic glycoside hydrolysis. Curr Opin Struct Biol 4:885–892

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Paes G, Berrin JG, Beaugrand J (2012) GH11 xylanases: structure/function/properties relationships and applications. Biotechnol Adv 30:564–592

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Rye CS, Withers SG (2000) Glycosidase mechanisms. Curr Opin Chem Biol 4:573–580

    Article  CAS  Google Scholar 

  • Sanchez C (2008) Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol Adv 27:185–194

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Schulze E (1891) Information regarding chemical composition of plant cell membrane. Ber Dtsch Chem Ges 24:2277–2287

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Singh S, Madlala AM, Prior BA (2003) Thermomyces lanuginosus: properties of strains and their hemicellulases. FEMS Microbiol Rev 27:3–16

    Article  CAS  Google Scholar 

  • Sunna A, Antranikian G (1997) Xylanolytic enzymes from fungi and bacteria. Crit Rev Biotechnol 17:39–67

    Article  CAS  Google Scholar 

  • Tenkanen M, Viikari L, Buchert J (1997) Use of acid-tolerant xylanase for bleaching of kraft pulps. Biotechnol Tech 11:935–993

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Törrönen A, Rouvinen J (1995) Structural comparison of two major endo-1,4-xylanases from Trichoderma reesei. Biochemistry 34:847–856

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Uffen RL (1997) Xylan degradation: a glimpse at microbial diversity. J Ind Microbiol Biotechnol 19:1–6

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Viikari L, Kantelinen A, Sundquist J, Linko M (1994) Xylanases in bleaching, from an idea to the industry. FEMS Microbiol Rev 13:335–350

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zechel DL, Withers SG (2000) Glycosidase mechanisms: anatomy of a finely tuned catalyst. Acc Chem Res 33:11–18

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

Download references

Acknowledgements

PD is thankful to the University Grant Commission, India and Visva-Bharati University for financial assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Amit Roy.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-018-1091-8

Keywords

Navigation