Skip to main content
SpringerLink
Log in

Thermostable microbial xylanases for pulp and paper industries: trends, applications and further perspectives

  • REVIEW
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Xylanases are enzymes with biotechnological relevance in a number of fields, including food, feed, biofuel, and textile industries. Their most significant application is in the paper and pulp industry, where they are used as a biobleaching agent, showing clear economic and environmental advantages over chemical alternatives. Since this process requires high temperatures and alkali media, the identification of thermostable and alkali stable xylanases represents a major biotechnological goal in this field. Moreover, thermostability is a desirable property for many other applications of xylanases. The review makes an overview of xylanase producing microorganisms and their current implementation in paper biobleaching. Future perspectives are analyzed focusing in the efforts carried out to generate thermostable enzymes by means of modern biotechnological tools, including metagenomic analysis, enzyme molecular engineering and nanotechnology. Furthermore, structural and mutagenesis studies have revealed critical sites for stability of xylanases from glycoside hydrolase families GH10 and GH11, which constitute the main classes of these enzymes. The overall conclusions of these works are summarized here and provide relevant information about putative weak spots within xylanase structures to be targeted in future protein engineering approaches.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59(1):143–169

    CAS  Google Scholar 

  • Amare G (1998) Purification and properties of two thermostable alkaline xylanases from an alkaliphilic Bacillus sp. Appl Environ Microbiol 64:3533–3535

    Google Scholar 

  • An J, Xie Y, Zhang Y et al (2015) Characterization of a thermostable, specific GH10 xylanase from Caldicellulosiruptor bescii with high catalytic activity. J Mol Catal B Enzym 117:13–20

    Article  CAS  Google Scholar 

  • Andrews SI, Taylor EJ, Pell G et al (2004) The use of forced protein evolution to investigate and improve stability of family 10 xylanases. The production of Ca2+-independent stable xylanases. J Biol Chem 279:54369–54379

    Article  CAS  Google Scholar 

  • Ayadi DZ, Sayari AH, Hlima HB et al (2015) Improvement of Trichoderma reesei xylanase II thermal stability by serine to threonine surface mutations. Int J Biol Macromol 72:163–170

    Article  Google Scholar 

  • Bajpai P (2012) Environmentally benign approaches for pulp bleaching, 2nd edn. Elsevier, New York

    Google Scholar 

  • Battan B, Sharma J, Dhiman SS, Kuhad RC (2007) Enhanced production of cellulase-free thermostable xylanase by Bacillus pumilus ASH and its potential application in paper industry. Enzyme Microb Technol 41(6–7):733–739

    Article  CAS  Google Scholar 

  • Bhardwaj A, Leelavathi S, Mazumdar-Leighton S et al (2008) The critical role of partially exposed N-terminal valine residue in stabilizing GH10 xylanase from Bacillus sp. NG-27 under poly-extreme conditions. PLoS One 26:e3063. doi:10.1371/journal.pone.0003063

    Article  Google Scholar 

  • Breccia JD, Sineriz F, Baigori MD, Castro GR, Hatti KR (1998) Purification and characterization of a thermostable xylanase from Bacillus amyloliquefaciens. Enzyme Microb Technol 22:42–49

    Article  CAS  Google Scholar 

  • Cannio R, Di Prizito N, Rossi M, Morana A (2004) A xylan-degrading strain of Sulfolobus solfataricus isolation & characterization of the xylanase activity. Extremophiles 8:117–124

    Article  CAS  Google Scholar 

  • Chanwicha N, Katekaew S, Aimi T, Boonlue S (2015) Purification and characterization of alkaline xylanase from Thermoascus aurantiacus var. levisporus KKU-PN-I2-1 cultivated by solid-state fermentation. Mycoscience 56(3):309–318

    Article  CAS  Google Scholar 

  • Chen CC, Luo H, Han X et al (2014) Structural perspectives of an engineered β-1,4-xylanase with enhanced thermostability. J Biotechnol 189:175–182

    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 

  • Dhiman SS, Kalyani D, Jagtap SS et al (2013) Characterization of a novel xylanase from Armillaria gemina and its immobilization onto SiO2 nanoparticles. Appl Microbiol Biotechnol 97:1081–1091

    Article  CAS  Google Scholar 

  • Du Y, Shi P, Huang H et al (2013) Characterization of three novel thermophilic xylanases from Humicola insolens Y1 with application potentials in the brewing industry. Bioresour Technol 130:161–167

    Article  CAS  Google Scholar 

  • Gallardo O, Pastor FI, Polaina J, Diaz P, Łysek R, Vogel P, Isorna P, González B, Sanz-Aparicio J (2010) Structural insights into the specificity of Xyn10B from Paenibacillus barcinonensis and its improved stability by forced protein evolution. J Biol Chem 285:2721–2733

    Article  CAS  Google Scholar 

  • Garg G, Dhiman SS, Mahajan R, Kaur A, Sharma J (2011) Bleach-boosting effect of crude xylanase from Bacillus stearothermophilus SDX on wheat straw pulp. New Biotechnol 28(1):58–64

    Article  CAS  Google Scholar 

  • Georis J, de Lemos Esteves F, Lamotte-Brasseur J et al (2000) An additional aromatic interaction improves the thermostability and thermophilicity of a mesophilic family 11 xylanase: structural basis and molecular study. Protein Sci 9:466–475

    Article  CAS  Google Scholar 

  • Ghatora SK, Chadha BS, Badhan AK, Saini HS, Bhat MK (2006) Identification and characterization of diverse xylanases from thermophlic and thermotolerant fungi. BioResources 1:18–33

    Google Scholar 

  • Hakulinen N, Turunen O, Jaenis J, Leisola M, Rouvinen J (2003) Three-dimensional structures of thermophilic beta-1,4-xylanases from Chaetomium thermophilum and Nonomuraea flexuosa. Comparison of twelve xylanases in relation to their thermal Stability. Eur J Biochem 270:1399–1412

    Article  CAS  Google Scholar 

  • Hokanson CA, Cappuccilli G, Odineca T et al (2011) Engineering highly thermostable xylanase variants using an enhanced combinatorial library method. Protein Eng Des Sel 24:597–605

    Article  CAS  Google Scholar 

  • Kamondi S, Szilágyi A, Barna L, Závodszky P (2008) Engineering the thermostability of a TIM-barrel enzyme by rational family shuffling. Biochem Biophys Res Commun 374:725–730

    Article  CAS  Google Scholar 

  • Kanokratana P, Eurwilaichitr L, Pootanakit K, Champreda V (2015) Identification of glycosyl hydrolases from a metagenomic library of microflora in sugarcane bagasse collection site and their cooperative action on cellulose degradation. J Biosci Bioeng 119(4):384–391

    Article  CAS  Google Scholar 

  • Kim HM, Lee KH, Kim KH, Lee DS, Nguyen QA, Bae HJ (2014) Efficient function and characterization of GH10 xylanase (Xyl10 g) from Gloeophyllum trabeum in lignocellulose degradation. J Biotechnol 172:31–45

    Article  Google Scholar 

  • Ko CH, Tsai CH, Tu J, Lee HY, Ku LT, Kuo PA, Lai YK (2010) Molecular cloning and characterization of a novel thermostable xylanase from Paenibacillus campinasensis BL11. Process Biochem 45:1638–1644

    Article  CAS  Google Scholar 

  • Kumar V, Verma D, Archana A, Satyanarayana T (2013) Thermostable bacterial xylanases. In: Satyanarayana T, Littlechild J, Kawarabayasi Y (eds) Thermophilic microbes in environmental and industrial biotechnology. Springer, New York, pp 813–857

    Chapter  Google Scholar 

  • Kumar V, Pandey P, Gupta S, Shukla P (2014) A reviving preliminary evoke on few xylanase producing fungal isolates from different ecological niche. Int J Curr Microbiol App Sci 3(4):501–506

    Google Scholar 

  • Landarani-Isfahani A, Taheri-Kafrani A, Amini M et al (2015) Xylanase immobilized on novel multifunctional hyperbranched polyglycerol-grafted magnetic nanoparticles: an Efficient and Robust Biocatalyst. Langmuir 31:9219–9227

    Article  CAS  Google Scholar 

  • Li XT, Jiang ZQ, Li LT et al (2005) Characterization of a cellulase-free neutral xylanase from Thermomyces lanuginosus CBS 288.54 and its biobleaching effect on wheat straw pulp. Bioresour Technol 96(12):1370–1379

    Article  CAS  Google Scholar 

  • Li H, Kankaanpää A, Xiong H et al (2013) Thermostabilization of extremophilic Dictyoglomus thermophilum GH11 xylanase by an N-terminal disulfide bridge and the effect of ionic liquid [emim]OAc on the enzymatic performance. Enzyme Microb Technol 53(6–7):414–419

    Article  Google Scholar 

  • Lin X, Han S, Zhang N et al (2013) Bleach boosting effect of xylanase A from Bacillus halodurans C-125 in ECF bleaching of wheat strawpulp. Enzyme Microb Technol 52(2):91–98

    Article  CAS  Google Scholar 

  • Liu L, Zhang G, Zhang Z, Wang S, Chen H (2011) Terminal amino acids disturb xylanase thermostability and activity. J Biol Chem 286:44710–44715

    Article  CAS  Google Scholar 

  • Liu M, Dai X, Guan R, Xin X (2014) Immobilization of Aspergillus niger xylanase A on Fe3O4-coated chitosan magnetic nanoparticles for xylooligosaccharide preparation. Catal Commun 55:6–10

    Article  CAS  Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy). Nucleic Acids Res 42:D490–D495

    Article  CAS  Google Scholar 

  • Maalej-Achouri I, Guerfali M, Romdhane IBB, Gargouri A, Belghith H (2012) The effect of Talaromyces thermophilus cellulase-free xylanase and commercial laccase on lignocellulosic components during the bleaching of kraft pulp. Int Biodeterior Biodegrad 75:43–48

    Article  CAS  Google Scholar 

  • Mamo G, Hatti-Kaul R, Mattiasson B (2006) A thermostable alkaline active endo-β-1-4-xylanase from Bacillus halodurans S7: purification and characterization. Enzyme Microb Technol 39(7):1492–1498

    Article  CAS  Google Scholar 

  • Mientus M, Brady S, Angelov A, Zimmermann P, Wemheuer B, Schuldes J, Daniel R, Liebl W (2015) Thermostable xylanase and β-glucanase derived from the metagenome of the avachinsky crater in kamchatka (Russia). Curr Biotechnol 2(4):284–293

    Article  Google Scholar 

  • Miyazaki K, Takenouchi M, Kondo H et al (2006) Thermal stabilization of Bacillus subtilis family-11 xylanase by directed evolution. J Biol Chem 281:10236–10242

    Article  CAS  Google Scholar 

  • Motta FL, Andrade CCP, Santana MHA (2013) A review of Xylanase Production by the fermentation of Xylan: classification, characterization and applications. In: Chandel AK, da Silva SS (eds) Sustainable degradation of lignocellulosic biomass-techniques, applications and commercialization. INTECH, Chennai, pp 251–275

    Google Scholar 

  • Ninawe S, Kuhad RC (2006) Bleaching of wheat straw-rich soda pulp with xylanase from a thermoalkalophilic Streptomyces cyaneus SN32. Bioresour Technol 97(18):2291–2295

    Article  CAS  Google Scholar 

  • Polizeli ML, Rizzatti AC, Monti R et al (2005) Xylanases from fungi: properties and industrial applications. Appl Microbiol Biotechnol 67:577–591

    Article  CAS  Google Scholar 

  • Qian C, Liu N, Yan X et al (2015) Engineering a high-performance, metagenomic-derived novelxylanase with improved soluble protein yield and thermostability. Enzyme Microb Technol 70:35–41

    Article  CAS  Google Scholar 

  • Roncero MB, Torres AL, Colom JF, Vidal T (2003) Effect of xylanase on ozone bleaching kinetics and properties of eucalyptus kraft pulp. J Chem Technol Biotechnol 78:1023–1031

    Article  CAS  Google Scholar 

  • Saleem M, Tabassum MR, Yasmin R, Imran M (2009) Potential of xylanase from thermophilic Bacillus sp. XTR-10 in biobleaching of wood kraft pulp. Int Biodeterior Biodegrad 63(8):1119–1124

    Article  CAS  Google Scholar 

  • Salles BC, Cunha RB, Fontes W, Sousa MV, Filho EXF (2000) Purification and characterization of a new xylanase Acrophialophora nainiana. J Biotechnol 81:199–204

    Article  CAS  Google Scholar 

  • Sharma M, Chadha BS, Saini HS (2010) Purification and characterization of two thermostable xylanases from Malbranchea flava active under alkaline conditions. Bioresour Technol 101(22):8834–8842

    Article  CAS  Google Scholar 

  • Sharma P, Sood C, Singh G, Capalash N (2015) An eco-friendly process for biobleaching of eucalyptus kraft pulp with xylanase producing Bacillus halodurans. J Clean Prod 87:966–970

    Article  CAS  Google Scholar 

  • Shibuya H, Kaneko S, Hayashi K (2000) Enhancement of the thermostability and hydrolytic activity of xylanase by random gene shuffling. Biochem J 15:651–656

    Article  Google Scholar 

  • Shrinivas D, Savitha G, Raviranjan K, Naik GR (2010) A highly thermostable alkaline cellulase-free xylanase from thermoalkalophilic Bacillus sp. JB 99 suitable for paper and pulp industry: purification and characterization. Appl Biochem Biotechnol 162(7):2049–2057

    Article  CAS  Google Scholar 

  • Shrivastava S, Lata S, Shukla P (2012) An insight on recent advances on immobilization methods for Industrial enzymes and its relevance to xylanases. Dyn Biochem Process Biotech Mol Biol 6(1):57–61

    Google Scholar 

  • Shrivastava S, Shukla P, Deepalakshmi PD, Mukhopadhyay K (2013) Characterization, cloning and functional expression of novel xylanase from Thermomyces lanuginosus SS-8 isolated from self-heating plant wreckage material. World J Microbiol Biotechnol 12:2407–2415

    Article  Google Scholar 

  • Song L, Tsang A, Sylvestre M (2015) Engineering a thermostable fungal GH10 xylanase, importance of N-terminal amino acids. Biotechnol Bioeng 112:1081–1091

    Article  CAS  Google Scholar 

  • Soozanipour A, Taheri-Kafrani A, Isfahani AL (2015) Covalent attachment of xylanase on functionalized magnetic nanoparticles and determination of its activity and stability. Chem Eng J 270:235–243

    Article  CAS  Google Scholar 

  • Sriprang R, Asano K, Gobsuk J et al (2006) Improvement of thermostability of fungal xylanase by using site-directed mutagenesis. J Biotechnol 126:454–462

    Article  CAS  Google Scholar 

  • Stephens DE, Khan FI, Singh P et al (2014) Creation of thermostable and alkaline stable xylanase variants by DNA shuffling. J Biotechnol 187:139–146

    Article  CAS  Google Scholar 

  • Sun JY, Liu MQ, Xu YL et al (2005) Improvement of the thermostability and catalytic activity of a mesophilic family 11 xylanase by N-terminus replacement. Protein Express Purif 42:122–130

    Article  CAS  Google Scholar 

  • Sun MZ, Zheng HC, Meng LC et al (2015) Direct cloning, expression of a thermostable xylanase gene from the metagenomic DNA of cow dung compost and enzymatic production of xylooligosaccharides from corncob. Biotechnol Lett 37:1877–1886

    Article  CAS  Google Scholar 

  • Sunna A, Bergquist PL (2003) A gene encoding a novel extremely thermostable 1,4-β xylanase isolated directly from an environmental DNA sample. Extremophiles 7:63–70

    CAS  Google Scholar 

  • Taneja K, Gupta S, Kuhad RC (2002) Properties and application of a partially purified alkaline xylanase from an alkalophilic fungus Aspergillus nidulans KK-99. Bioresour Technol 85(1):39–42

    Article  CAS  Google Scholar 

  • Turunen O, Etuaho K, Fenel F et al (2001) A combination of weakly stabilizing mutations with a disulfide bridge in the alpha-helix region of Trichoderma reesei endo-1,4-beta-xylanase II increases the thermal stability through synergism. J Biotechnol 88:37–46

    Article  CAS  Google Scholar 

  • Turunen O, Vuorio M, Fenel F, Leisola M (2002) Engineering of multiple arginines into the Ser/Thr surface of Trichoderma reesei endo-1,4-beta-xylanase II increases the thermotolerance and shifts the pH optimum towards alkaline pH. Protein Eng 15:141–145

    Article  CAS  Google Scholar 

  • Verma D, Kawarabayasi Y, Miyazaki K, Satyanarayana T (2013) Cloning, expression and characteristics of a novel alkalistable and thermostable xylanase encoding gene (Mxyl) retrieved from compost-soil metagenome. PLoS One 8(1):e52459. doi:10.1371/journal.pone.0052459

    Article  CAS  Google Scholar 

  • Wakarchuk WW, Sung WL, Campbell RL et al (1994) Thermostabilization of the Bacillus circulans xylanase by the introduction of disulfide bonds. Protein Eng 7:1379–1386

    Article  CAS  Google Scholar 

  • Wang K, Luo H, Tian J et al (2014) Thermostability improvement of a streptomyces xylanase by introducing proline and glutamic acid residues. Appl Environ Microbiol 80:2158–2165

    Article  Google Scholar 

  • Xie H, Flint J, Vardakou M et al (2006) Probing the structural basis for the difference in thermostability displayed by family 10 xylanases. J Mol Biol 360:157–167

    Article  CAS  Google Scholar 

  • Xiong H, Fenel F, Leisola M, Turunen O (2004) Engineering the thermostability of Trichoderma reesei endo-1,4-beta-xylanase II by combination of disulphide bridges. Extremophiles 8:393–400

    Article  CAS  Google Scholar 

  • Yang X, Shi P, Huang H, Luo H, Wang Y, Zhang W, Yao B (2014) 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 148:381–387

    Article  CAS  Google Scholar 

  • Zhang F, Chen JJ, Ren WZ, Lin LB, Zhou Y, Zhi XY, Tang SK, Li WJ (2012) Cloning, expression, and characterization of an alkaline thermostable GH11 xylanase from Thermobifida halotolerans YIM 90462T. J Ind Microbiol Biotechnol 39:1109–1116

    Article  CAS  Google Scholar 

  • Zhang S, He Y, Yu H, Dong Z (2014) Seven N-terminal residues of a thermophilic xylanases are sufficient to confer hyperthermostability on its mesophilic counterpart. PLoS One 9:e87632. doi:10.1371/journal.pone.0087632

    Article  Google Scholar 

  • Zheng H, Liu Y, Liu X et al (2012) Overexpression of a Paenibacillus campinasensis xylanase in Bacillus megaterium and its applications to biobleaching of cotton stalk pulp and saccharification of recycled paper sludge. Bioresour Technol 125:182–187

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge the support from SERB, Department of Science and Technology, Government of India (DST Fast Track Grant No. SR/FT/LS-31/2012), University Grants Commission (UGC), New Delhi, India (Grant No. 42-457/2013 (SR) and Grant BIO2013-48779-C4-3-R from Spain’s State Secretariat for Research, Development and Innovation (Ministry of Economy and Competitiveness). Vishal Kumar is thankful to UGC New Delhi, India for awarding Junior Research Fellowship [F.17-63/2008 (SA-I)].

Author information

Authors and Affiliations

  1. Enzyme Technology and Protein Bioinformatics Laboratory, Department of Microbiology, Maharshi Dayanand University, Rohtak, Haryana, 124001, India

    Vishal Kumar & Pratyoosh Shukla

  2. Instituto de Agroquímica y Tecnología de Alimentos, C.S.I.C., Av. Catedrático Agustín Escardino, 7, E6980, Paterna, Valencia, Spain

    Julia Marín-Navarro

Authors
  1. Vishal Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Julia Marín-Navarro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pratyoosh Shukla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pratyoosh Shukla.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, V., Marín-Navarro, J. & Shukla, P. Thermostable microbial xylanases for pulp and paper industries: trends, applications and further perspectives. World J Microbiol Biotechnol 32, 34 (2016). https://doi.org/10.1007/s11274-015-2005-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-015-2005-0

Keywords

Search

Navigation