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Immobilization of Thermomyces lanuginosus Xylanase on Aluminum Hydroxide Particles Through Adsorption: Characterization of Immobilized Enzyme
1College of Resources and Environmental Sciences, Henan Agricultural University, Zhengzhou 450000, P.R. China, 2College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, P.R. China, 3Soil and Fertilizer Bureau of Shandong Province, Shandong 253016, P.R. China
J. Microbiol. Biotechnol. 2015; 25(12): 2016-2023
Published December 28, 2015 https://doi.org/10.4014/jmb.1502.02046
Copyright © The Korean Society for Microbiology and Biotechnology.
Abstract
Keywords
References
- Ahn MY, Zimmerman AR, Martínez CE, Archibald DD, Bollag JM, Dec J. 2007. Characteristics of Trametes villosa laccase adsorbed on aluminum hydroxide. Enzyme Microb. Technol. 41: 141-148.
- Ai Z, Jiang Z, Li L, Deng W, Kusakabe I, Li H. 2005. Immobilization of Streptomyces olivaceoviridis E-86 xylanase on Eudragit S-100 for xylo-oligosaccharide production. Process Biochem. 40: 2707-2714.
- Ansari SA, Husain Q. 2012. Potential applications of enzymes immobilized on/in nano materials: a review. Biotechnol. Adv. 30: 512-523.
- Bailey MJ, Biely P, Poutanen K. 1992. Interlaboratory testing of methods for assay of xylanase activity. J. Biotechnol. 23:257-270.
- Bayramoglu G, Akgöl S, Bulut A, Denizli A, Yakup Arýca M. 2003. Covalent immobilisation of invertase onto a reactive film composed of 2-hydroxyethyl methacrylate and glycidyl methacrylate: properties and application in a continuous flow system. Biochem. Eng. J. 14: 117-126.
- Bennett NA, Ryan J, Biely P, Vrsanska M, Kremnicky L, Macris BJ, et al. 1998. Biochemical and catalytic properties of an endoxylanase purified from the culture filtrate of Thermomyces lanuginosus ATCC 46882. Carbohydr. Res. 306: 445-455.
- Buchholz K, Kasche V, Bornscheuer UT. 2012. Biocatalysts and Enzyme Technology. John Wiley & Sons, NY.
- Cesar T, Mrša V. 1996. Purification and properties of the xylanase produced by Thermomyces lanuginosus. Enzyme Microb. Technol. 19: 289-296.
- Chen H, Liu L, Lv S, Liu X, Wang M, Song A, Jia X. 2010. Immobilization of Aspergillus niger xylanase on chitosan using dialdehyde starch as a coupling agent. Appl. Biochem. Biotechnol. 162: 24-32.
- Dhiman SS, Sharma J, Battan B. 2008. Industrial applications and future prospects of microbial xylanases: a review. BioResources 3: 1377-1402.
- Driss D, Zouari-Ellouzi S, Chaari F, Kallel F, Ghazala I, Bouaziz F, Chaabouni SE. 2014. Production and in vitro evaluation of xylooligosaccharides generated from corncobs using immobilized Penicillium occitanis xylanase. J. Mol. Catal. B Enzym. 102: 146-153.
- Edward VA, Pillay VL, Swart P, Singh S. 2002. Immobilization of xylanase from Thermomyces lanuginosus SSBP using Eudragit S-100: research in action. S. Afr. J. Sci. 98: 553-554.
- Garcia-Galan C, Berenguer-Murcia Á, Fernandez-Lafuente R, Rodrigues RC. 2011. Potential of different enzyme immobilization strategies to improve enzyme performance. Adv. Synth. Catal. 353: 2885-2904.
- Gaur R, Khare S. 2005. Immobilization of xylan-degrading enzymes from Scytalidium thermophilum on Eudragit L-100. World J. Microbiol. Biotechnol. 21: 1123-1128.
- Gouda MK, Abdel-Naby MA. 2002. Catalytic properties of the immobilized Aspergillus tamarii xylanase. Microbiol. Res. 157: 275-281.
- Gustafsson H, Johansson EM, Barrabino A, Odén M, Holmberg K. 2012. Immobilization of lipase from Mucor miehei and Rhizopus oryzae into mesoporous silica: the effect of varied particle size and morphology. Colloids Surf. B Biointerfaces 100: 22-30.
- Illanes A. 2008. Enzyme Biocatalysis: Principles and Applications. Springer Science & Business Media, Berlin.
- Jesionowski T, Zdarta J, Krajewska B. 2014. Enzyme immobilization by adsorption: a review. Adsorption 20: 801-821.
- Juturu V, Wu JC. 2012. Microbial xylanases: engineering, production and industrial applications. Biotechnol. Adv. 30:1219-1227.
- Kapoor M, Kuhad RC. 2007. Immobilization of xylanase from Bacillus pumilus strain MK001 and its application in production of xylo-oligosaccharides. Appl. Biochem. Biotechnol. 142: 125-138.
- Kyle J, Posner A, Quirk J. 1975. Kinetics of isotopic exchange of phosphate adsorbed on gibbsite. J. Soil Sci. 6: 32-43.
- Lammirato C, Miltner A, Wick LY, Kästner M. 2010. Hydrolysis of cellobiose by β-glucosidase in the presence of soil minerals: interactions at solid–liquid interfaces and effects on enzyme activity levels. Soil Biol. Biochem. 42: 2203-2210.
- Li L, Zhu Y, Huang Z, Jiang Z, Chen W. 2007. Immobilization of the recombinant xylanase B (XynB) from the hyperthermophilic Thermotoga maritima on metal-chelate Eupergit C 250L. Enzyme Microb. Technol. 41: 278-285.
- Liese A, Hilterhaus L. 2013. Evaluation of immobilized enzymes for industrial applications. Chem. Soc. Rev. 42:6236-6249.
- Lin YS, Tseng MJ, Lee WC. 2011. Production of xylooligosaccharides using immobilized endo-xylanase of Bacillus halodurans. Process Biochem. 46: 2117-2121.
- Liu MQ, Dai XJ, Guan RF, Xu X. 2014. Immobilization of Aspergillus niger xylanase A on Fe3O4-coated chitosan magnetic nanoparticles for xylooligosaccharides preparation. Catal. Commun. 55: 6-10.
- Manning BA, Goldberg S. 1997. Adsorption and stability of arsenic(III) at the clay mineral-water interface. Environ. Sci. Technol. 31: 2005-2011.
- Manrich A, Komesu A, Adriano WS, Tardioli PW, Giordano RLC. 2010. Immobilization and stabilization of xylanase by multipoint covalent attachment on agarose and on chitosan supports. Appl. Biochem. Biotechnol. 161: 455-467.
- Milka P, Krest I, Keusgen M. 2000. Immobilization of alliinase on porous aluminum oxide. Biotechnol. Bioeng. 69: 344-348.
- Nagar S, Mittal A, Gupta VK. 2014. Two w ay s trategy for utilizing agricultural waste ‘wheat bran’ for production and immobilization of xylanase. J. Innov. Biol. 1: 035-044.
- Nagar S, Mittal A, Kumar D, Kumar L, Gupta VK. 2012. Immobilization of xylanase on glutaraldehyde activated aluminum oxide pellets for increasing digestibility of poultry feed. Process Biochem. 47: 1402-1410.
- Nestl BM, Nebel BA, Hauer B. 2011. Recent progress in industrial biocatalysis. Curr. Opin. Chem. Biol. 15: 187-193.
- Ortega N, Perez-Mateos M, Pilar MaC, Busto MaD. 2008. Neutrase immobilization on alginate-glutaraldehyde beads by covalent attachment. J. Agric. food Chem. 57: 109-115.
- Osman B, Kara A, Uzun L, Be irli N, Denizli A. 2005. Vinyl imidazole carrying metal-chelated beads for reversible use in yeast invertase adsorption. J. Mol. Catal. B Enzym. 37: 88-94.
- Pal A, Khanum F. 2011. Covalent immobilization of xylanase on glutaraldehyde activated alginate beads using response surface methodology: characterization of immobilized enzyme. Process Biochem. 46: 1315-1322.
- Qiu H, Xu C, Huang X, Ding Y, Qu Y, Gao P. 2009. Immobilization of laccase on nanoporous gold: comparative studies on the immobilization strategies and the particle size effects. J. Phys. Chem. C 113: 2521-2525.
- Quiquampoix H. 2000. Mechanisms of protein adsorption on surfaces and consequences for extracellular enzyme activity in soil. Soil Biochem. 10: 171-206.
- Quiquampoix H, Servagent-Noinville S, Baron MH. 2002. Enzyme adsorption on soil mineral surfaces and consequences for the catalytic activity, pp. 285-306. In: Enzymes in the Environment. Marcel Dekker, New York.
- Quiquampoix H, Staunton S, Baron MH, Ratcliffe R. 1993. Interpretation of the pH dependence of protein adsorption on clay mineral surfaces and its relevance to the understanding of extracellular enzyme activity in soil. Colloids Surf. A Physicochem. Eng. Asp. 75: 85-93.
- Reshmi R, Sanjay G, Sugunan S. 2006. Enhanced activity and stability of α-amylase immobilized on alumina. Catal. Commun. 7: 460-465.
- Sheldon RA. 2007. Enzyme immobilization: the quest for optimum performance. Adv. Synth. Catal. 349: 1289-1307.
- 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.
- Tietjen T, Wetzel RG. 2003. Extracellular enzyme-clay mineral complexes: enzyme adsorption, alteration of enzyme activity, and protection from photodegradation. Aquat. Ecol. 37: 331-339.
- Wefers K, Misra C. 1987. Oxides and hydroxides of aluminum. Technical Paper No. 19. Alcoa Laboratories, Pittsburgh, PA.
- Wohlgemuth R. 2010. Asymmetric biocatalysis with microbial enzymes and cells. Curr. Opin. Microbiol. 13: 283-292.
- Wu Y, Jiang Y, Jiao J, Liu M, Hu F, Griffiths BS, Li H. 2014. Adsorption of Trametes versicolor laccase to soil iron and aluminum minerals: enzyme activity, kinetics and stability studies. Colloids Surf. B Biointerfaces 114: 342-348.
- Yan X, Wang X, Zhao P, Xu P, Ding Y. 2012. Xylanase immobilized nanoporous gold as a highly active and stable biocatalyst. Microporous Mesoporous Mater. 161: 1-6.
- Zhu J, Huang Q, Pigna M, Violante A. 2010. Immobilization of acid phosphatase on uncalcined and calcined Mg/Al-CO3 layered double hydroxides. Colloids Surf. B Biointerfaces 77:166-173.
Related articles in JMB

Article
Research article
J. Microbiol. Biotechnol. 2015; 25(12): 2016-2023
Published online December 28, 2015 https://doi.org/10.4014/jmb.1502.02046
Copyright © The Korean Society for Microbiology and Biotechnology.
Immobilization of Thermomyces lanuginosus Xylanase on Aluminum Hydroxide Particles Through Adsorption: Characterization of Immobilized Enzyme
Ying Jiang 1, Yue Wu 2, 3 and Huixin Li 2*
1College of Resources and Environmental Sciences, Henan Agricultural University, Zhengzhou 450000, P.R. China, 2College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, P.R. China, 3Soil and Fertilizer Bureau of Shandong Province, Shandong 253016, P.R. China
Abstract
Xylanase plays important roles in a broad range of industrial production as a biocatalyst, and
its applications commonly require immobilization on supports to enhance its stability.
Aluminum hydroxide, a carrier material with high surface area, has the advantages of simple
and low-cost preparation and resistance to biodegradation, and can be potentially used as a
proper support for xylanase immobilization. In this work, xylanase from Thermomyces
lanuginosus was immobilized on two types of aluminum hydroxide particles (gibbsite and
amorphous Al(OH)3) through adsorption, and the properties of the adsorbed enzymes were
studied. Both particles had considerable adsorptive capacity and affinity for xylanase.
Xylanase retained 75% and 64% of the original catalytic activities after adsorption to gibbsite
and amorphous Al(OH)3. Both the adsorptions improved pH and thermal stability, lowered
activation energy, and extended lifespan of the immobilized enzyme, as compared with the
free enzyme. Xylanase adsorbed on gibbsite and amorphous Al(OH)3 retained 71% and 64% of
its initial activity, respectively, after being recycled five times. These results indicated that
aluminum hydroxides served as good supports for xylanase immobilization. Therefore, the
adsorption of xylanase on aluminum hydroxide particles has promising potential for practical
production.
Keywords: Xylanase, Gibbsite, Amorphous Al(OH)3, Adsorption, Catalytic performance
References
- Ahn MY, Zimmerman AR, Martínez CE, Archibald DD, Bollag JM, Dec J. 2007. Characteristics of Trametes villosa laccase adsorbed on aluminum hydroxide. Enzyme Microb. Technol. 41: 141-148.
- Ai Z, Jiang Z, Li L, Deng W, Kusakabe I, Li H. 2005. Immobilization of Streptomyces olivaceoviridis E-86 xylanase on Eudragit S-100 for xylo-oligosaccharide production. Process Biochem. 40: 2707-2714.
- Ansari SA, Husain Q. 2012. Potential applications of enzymes immobilized on/in nano materials: a review. Biotechnol. Adv. 30: 512-523.
- Bailey MJ, Biely P, Poutanen K. 1992. Interlaboratory testing of methods for assay of xylanase activity. J. Biotechnol. 23:257-270.
- Bayramoglu G, Akgöl S, Bulut A, Denizli A, Yakup Arýca M. 2003. Covalent immobilisation of invertase onto a reactive film composed of 2-hydroxyethyl methacrylate and glycidyl methacrylate: properties and application in a continuous flow system. Biochem. Eng. J. 14: 117-126.
- Bennett NA, Ryan J, Biely P, Vrsanska M, Kremnicky L, Macris BJ, et al. 1998. Biochemical and catalytic properties of an endoxylanase purified from the culture filtrate of Thermomyces lanuginosus ATCC 46882. Carbohydr. Res. 306: 445-455.
- Buchholz K, Kasche V, Bornscheuer UT. 2012. Biocatalysts and Enzyme Technology. John Wiley & Sons, NY.
- Cesar T, Mrša V. 1996. Purification and properties of the xylanase produced by Thermomyces lanuginosus. Enzyme Microb. Technol. 19: 289-296.
- Chen H, Liu L, Lv S, Liu X, Wang M, Song A, Jia X. 2010. Immobilization of Aspergillus niger xylanase on chitosan using dialdehyde starch as a coupling agent. Appl. Biochem. Biotechnol. 162: 24-32.
- Dhiman SS, Sharma J, Battan B. 2008. Industrial applications and future prospects of microbial xylanases: a review. BioResources 3: 1377-1402.
- Driss D, Zouari-Ellouzi S, Chaari F, Kallel F, Ghazala I, Bouaziz F, Chaabouni SE. 2014. Production and in vitro evaluation of xylooligosaccharides generated from corncobs using immobilized Penicillium occitanis xylanase. J. Mol. Catal. B Enzym. 102: 146-153.
- Edward VA, Pillay VL, Swart P, Singh S. 2002. Immobilization of xylanase from Thermomyces lanuginosus SSBP using Eudragit S-100: research in action. S. Afr. J. Sci. 98: 553-554.
- Garcia-Galan C, Berenguer-Murcia Á, Fernandez-Lafuente R, Rodrigues RC. 2011. Potential of different enzyme immobilization strategies to improve enzyme performance. Adv. Synth. Catal. 353: 2885-2904.
- Gaur R, Khare S. 2005. Immobilization of xylan-degrading enzymes from Scytalidium thermophilum on Eudragit L-100. World J. Microbiol. Biotechnol. 21: 1123-1128.
- Gouda MK, Abdel-Naby MA. 2002. Catalytic properties of the immobilized Aspergillus tamarii xylanase. Microbiol. Res. 157: 275-281.
- Gustafsson H, Johansson EM, Barrabino A, Odén M, Holmberg K. 2012. Immobilization of lipase from Mucor miehei and Rhizopus oryzae into mesoporous silica: the effect of varied particle size and morphology. Colloids Surf. B Biointerfaces 100: 22-30.
- Illanes A. 2008. Enzyme Biocatalysis: Principles and Applications. Springer Science & Business Media, Berlin.
- Jesionowski T, Zdarta J, Krajewska B. 2014. Enzyme immobilization by adsorption: a review. Adsorption 20: 801-821.
- Juturu V, Wu JC. 2012. Microbial xylanases: engineering, production and industrial applications. Biotechnol. Adv. 30:1219-1227.
- Kapoor M, Kuhad RC. 2007. Immobilization of xylanase from Bacillus pumilus strain MK001 and its application in production of xylo-oligosaccharides. Appl. Biochem. Biotechnol. 142: 125-138.
- Kyle J, Posner A, Quirk J. 1975. Kinetics of isotopic exchange of phosphate adsorbed on gibbsite. J. Soil Sci. 6: 32-43.
- Lammirato C, Miltner A, Wick LY, Kästner M. 2010. Hydrolysis of cellobiose by β-glucosidase in the presence of soil minerals: interactions at solid–liquid interfaces and effects on enzyme activity levels. Soil Biol. Biochem. 42: 2203-2210.
- Li L, Zhu Y, Huang Z, Jiang Z, Chen W. 2007. Immobilization of the recombinant xylanase B (XynB) from the hyperthermophilic Thermotoga maritima on metal-chelate Eupergit C 250L. Enzyme Microb. Technol. 41: 278-285.
- Liese A, Hilterhaus L. 2013. Evaluation of immobilized enzymes for industrial applications. Chem. Soc. Rev. 42:6236-6249.
- Lin YS, Tseng MJ, Lee WC. 2011. Production of xylooligosaccharides using immobilized endo-xylanase of Bacillus halodurans. Process Biochem. 46: 2117-2121.
- Liu MQ, Dai XJ, Guan RF, Xu X. 2014. Immobilization of Aspergillus niger xylanase A on Fe3O4-coated chitosan magnetic nanoparticles for xylooligosaccharides preparation. Catal. Commun. 55: 6-10.
- Manning BA, Goldberg S. 1997. Adsorption and stability of arsenic(III) at the clay mineral-water interface. Environ. Sci. Technol. 31: 2005-2011.
- Manrich A, Komesu A, Adriano WS, Tardioli PW, Giordano RLC. 2010. Immobilization and stabilization of xylanase by multipoint covalent attachment on agarose and on chitosan supports. Appl. Biochem. Biotechnol. 161: 455-467.
- Milka P, Krest I, Keusgen M. 2000. Immobilization of alliinase on porous aluminum oxide. Biotechnol. Bioeng. 69: 344-348.
- Nagar S, Mittal A, Gupta VK. 2014. Two w ay s trategy for utilizing agricultural waste ‘wheat bran’ for production and immobilization of xylanase. J. Innov. Biol. 1: 035-044.
- Nagar S, Mittal A, Kumar D, Kumar L, Gupta VK. 2012. Immobilization of xylanase on glutaraldehyde activated aluminum oxide pellets for increasing digestibility of poultry feed. Process Biochem. 47: 1402-1410.
- Nestl BM, Nebel BA, Hauer B. 2011. Recent progress in industrial biocatalysis. Curr. Opin. Chem. Biol. 15: 187-193.
- Ortega N, Perez-Mateos M, Pilar MaC, Busto MaD. 2008. Neutrase immobilization on alginate-glutaraldehyde beads by covalent attachment. J. Agric. food Chem. 57: 109-115.
- Osman B, Kara A, Uzun L, Be irli N, Denizli A. 2005. Vinyl imidazole carrying metal-chelated beads for reversible use in yeast invertase adsorption. J. Mol. Catal. B Enzym. 37: 88-94.
- Pal A, Khanum F. 2011. Covalent immobilization of xylanase on glutaraldehyde activated alginate beads using response surface methodology: characterization of immobilized enzyme. Process Biochem. 46: 1315-1322.
- Qiu H, Xu C, Huang X, Ding Y, Qu Y, Gao P. 2009. Immobilization of laccase on nanoporous gold: comparative studies on the immobilization strategies and the particle size effects. J. Phys. Chem. C 113: 2521-2525.
- Quiquampoix H. 2000. Mechanisms of protein adsorption on surfaces and consequences for extracellular enzyme activity in soil. Soil Biochem. 10: 171-206.
- Quiquampoix H, Servagent-Noinville S, Baron MH. 2002. Enzyme adsorption on soil mineral surfaces and consequences for the catalytic activity, pp. 285-306. In: Enzymes in the Environment. Marcel Dekker, New York.
- Quiquampoix H, Staunton S, Baron MH, Ratcliffe R. 1993. Interpretation of the pH dependence of protein adsorption on clay mineral surfaces and its relevance to the understanding of extracellular enzyme activity in soil. Colloids Surf. A Physicochem. Eng. Asp. 75: 85-93.
- Reshmi R, Sanjay G, Sugunan S. 2006. Enhanced activity and stability of α-amylase immobilized on alumina. Catal. Commun. 7: 460-465.
- Sheldon RA. 2007. Enzyme immobilization: the quest for optimum performance. Adv. Synth. Catal. 349: 1289-1307.
- 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.
- Tietjen T, Wetzel RG. 2003. Extracellular enzyme-clay mineral complexes: enzyme adsorption, alteration of enzyme activity, and protection from photodegradation. Aquat. Ecol. 37: 331-339.
- Wefers K, Misra C. 1987. Oxides and hydroxides of aluminum. Technical Paper No. 19. Alcoa Laboratories, Pittsburgh, PA.
- Wohlgemuth R. 2010. Asymmetric biocatalysis with microbial enzymes and cells. Curr. Opin. Microbiol. 13: 283-292.
- Wu Y, Jiang Y, Jiao J, Liu M, Hu F, Griffiths BS, Li H. 2014. Adsorption of Trametes versicolor laccase to soil iron and aluminum minerals: enzyme activity, kinetics and stability studies. Colloids Surf. B Biointerfaces 114: 342-348.
- Yan X, Wang X, Zhao P, Xu P, Ding Y. 2012. Xylanase immobilized nanoporous gold as a highly active and stable biocatalyst. Microporous Mesoporous Mater. 161: 1-6.
- Zhu J, Huang Q, Pigna M, Violante A. 2010. Immobilization of acid phosphatase on uncalcined and calcined Mg/Al-CO3 layered double hydroxides. Colloids Surf. B Biointerfaces 77:166-173.