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References

  1. 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.
    CrossRef
  2. 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.
    CrossRef
  3. Ansari SA, Husain Q. 2012. Potential applications of enzymes immobilized on/in nano materials: a review. Biotechnol. Adv. 30: 512-523.
    Pubmed CrossRef
  4. Bailey MJ, Biely P, Poutanen K. 1992. Interlaboratory testing of methods for assay of xylanase activity. J. Biotechnol. 23:257-270.
    CrossRef
  5. 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.
    CrossRef
  6. 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.
    CrossRef
  7. Buchholz K, Kasche V, Bornscheuer UT. 2012. Biocatalysts and Enzyme Technology. John Wiley & Sons, NY.
  8. Cesar T, Mrša V. 1996. Purification and properties of the xylanase produced by Thermomyces lanuginosus. Enzyme Microb. Technol. 19: 289-296.
    CrossRef
  9. 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.
    Pubmed CrossRef
  10. Dhiman SS, Sharma J, Battan B. 2008. Industrial applications and future prospects of microbial xylanases: a review. BioResources 3: 1377-1402.
  11. 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.
    CrossRef
  12. 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.
  13. 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.
    CrossRef
  14. Gaur R, Khare S. 2005. Immobilization of xylan-degrading enzymes from Scytalidium thermophilum on Eudragit L-100. World J. Microbiol. Biotechnol. 21: 1123-1128.
    CrossRef
  15. Gouda MK, Abdel-Naby MA. 2002. Catalytic properties of the immobilized Aspergillus tamarii xylanase. Microbiol. Res. 157: 275-281.
    Pubmed CrossRef
  16. 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.
    Pubmed CrossRef
  17. Illanes A. 2008. Enzyme Biocatalysis: Principles and Applications. Springer Science & Business Media, Berlin.
    CrossRef
  18. Jesionowski T, Zdarta J, Krajewska B. 2014. Enzyme immobilization by adsorption: a review. Adsorption 20: 801-821.
    CrossRef
  19. Juturu V, Wu JC. 2012. Microbial xylanases: engineering, production and industrial applications. Biotechnol. Adv. 30:1219-1227.
    Pubmed CrossRef
  20. 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.
    Pubmed CrossRef
  21. Kyle J, Posner A, Quirk J. 1975. Kinetics of isotopic exchange of phosphate adsorbed on gibbsite. J. Soil Sci. 6: 32-43.
    CrossRef
  22. 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.
    CrossRef
  23. 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.
    CrossRef
  24. Liese A, Hilterhaus L. 2013. Evaluation of immobilized enzymes for industrial applications. Chem. Soc. Rev. 42:6236-6249.
    Pubmed CrossRef
  25. Lin YS, Tseng MJ, Lee WC. 2011. Production of xylooligosaccharides using immobilized endo-xylanase of Bacillus halodurans. Process Biochem. 46: 2117-2121.
    CrossRef
  26. 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.
    CrossRef
  27. Manning BA, Goldberg S. 1997. Adsorption and stability of arsenic(III) at the clay mineral-water interface. Environ. Sci. Technol. 31: 2005-2011.
    CrossRef
  28. 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.
    Pubmed CrossRef
  29. Milka P, Krest I, Keusgen M. 2000. Immobilization of alliinase on porous aluminum oxide. Biotechnol. Bioeng. 69: 344-348.
    CrossRef
  30. 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.
  31. 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.
    CrossRef
  32. Nestl BM, Nebel BA, Hauer B. 2011. Recent progress in industrial biocatalysis. Curr. Opin. Chem. Biol. 15: 187-193.
    Pubmed CrossRef
  33. 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.
    Pubmed CrossRef
  34. 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.
    CrossRef
  35. 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.
    CrossRef
  36. 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.
    CrossRef
  37. Quiquampoix H. 2000. Mechanisms of protein adsorption on surfaces and consequences for extracellular enzyme activity in soil. Soil Biochem. 10: 171-206.
  38. 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.
    CrossRef
  39. 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.
    CrossRef
  40. Reshmi R, Sanjay G, Sugunan S. 2006. Enhanced activity and stability of α-amylase immobilized on alumina. Catal. Commun. 7: 460-465.
    CrossRef
  41. Sheldon RA. 2007. Enzyme immobilization: the quest for optimum performance. Adv. Synth. Catal. 349: 1289-1307.
    CrossRef
  42. 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.
    CrossRef
  43. 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.
    CrossRef
  44. Wefers K, Misra C. 1987. Oxides and hydroxides of aluminum. Technical Paper No. 19. Alcoa Laboratories, Pittsburgh, PA.
  45. Wohlgemuth R. 2010. Asymmetric biocatalysis with microbial enzymes and cells. Curr. Opin. Microbiol. 13: 283-292.
    Pubmed CrossRef
  46. 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.
    Pubmed CrossRef
  47. 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.
    CrossRef
  48. 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.
    Pubmed CrossRef

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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

Received: February 25, 2015; Accepted: August 11, 2015

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

  1. 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.
    CrossRef
  2. 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.
    CrossRef
  3. Ansari SA, Husain Q. 2012. Potential applications of enzymes immobilized on/in nano materials: a review. Biotechnol. Adv. 30: 512-523.
    Pubmed CrossRef
  4. Bailey MJ, Biely P, Poutanen K. 1992. Interlaboratory testing of methods for assay of xylanase activity. J. Biotechnol. 23:257-270.
    CrossRef
  5. 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.
    CrossRef
  6. 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.
    CrossRef
  7. Buchholz K, Kasche V, Bornscheuer UT. 2012. Biocatalysts and Enzyme Technology. John Wiley & Sons, NY.
  8. Cesar T, Mrša V. 1996. Purification and properties of the xylanase produced by Thermomyces lanuginosus. Enzyme Microb. Technol. 19: 289-296.
    CrossRef
  9. 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.
    Pubmed CrossRef
  10. Dhiman SS, Sharma J, Battan B. 2008. Industrial applications and future prospects of microbial xylanases: a review. BioResources 3: 1377-1402.
  11. 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.
    CrossRef
  12. 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.
  13. 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.
    CrossRef
  14. Gaur R, Khare S. 2005. Immobilization of xylan-degrading enzymes from Scytalidium thermophilum on Eudragit L-100. World J. Microbiol. Biotechnol. 21: 1123-1128.
    CrossRef
  15. Gouda MK, Abdel-Naby MA. 2002. Catalytic properties of the immobilized Aspergillus tamarii xylanase. Microbiol. Res. 157: 275-281.
    Pubmed CrossRef
  16. 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.
    Pubmed CrossRef
  17. Illanes A. 2008. Enzyme Biocatalysis: Principles and Applications. Springer Science & Business Media, Berlin.
    CrossRef
  18. Jesionowski T, Zdarta J, Krajewska B. 2014. Enzyme immobilization by adsorption: a review. Adsorption 20: 801-821.
    CrossRef
  19. Juturu V, Wu JC. 2012. Microbial xylanases: engineering, production and industrial applications. Biotechnol. Adv. 30:1219-1227.
    Pubmed CrossRef
  20. 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.
    Pubmed CrossRef
  21. Kyle J, Posner A, Quirk J. 1975. Kinetics of isotopic exchange of phosphate adsorbed on gibbsite. J. Soil Sci. 6: 32-43.
    CrossRef
  22. 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.
    CrossRef
  23. 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.
    CrossRef
  24. Liese A, Hilterhaus L. 2013. Evaluation of immobilized enzymes for industrial applications. Chem. Soc. Rev. 42:6236-6249.
    Pubmed CrossRef
  25. Lin YS, Tseng MJ, Lee WC. 2011. Production of xylooligosaccharides using immobilized endo-xylanase of Bacillus halodurans. Process Biochem. 46: 2117-2121.
    CrossRef
  26. 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.
    CrossRef
  27. Manning BA, Goldberg S. 1997. Adsorption and stability of arsenic(III) at the clay mineral-water interface. Environ. Sci. Technol. 31: 2005-2011.
    CrossRef
  28. 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.
    Pubmed CrossRef
  29. Milka P, Krest I, Keusgen M. 2000. Immobilization of alliinase on porous aluminum oxide. Biotechnol. Bioeng. 69: 344-348.
    CrossRef
  30. 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.
  31. 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.
    CrossRef
  32. Nestl BM, Nebel BA, Hauer B. 2011. Recent progress in industrial biocatalysis. Curr. Opin. Chem. Biol. 15: 187-193.
    Pubmed CrossRef
  33. 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.
    Pubmed CrossRef
  34. 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.
    CrossRef
  35. 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.
    CrossRef
  36. 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.
    CrossRef
  37. Quiquampoix H. 2000. Mechanisms of protein adsorption on surfaces and consequences for extracellular enzyme activity in soil. Soil Biochem. 10: 171-206.
  38. 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.
    CrossRef
  39. 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.
    CrossRef
  40. Reshmi R, Sanjay G, Sugunan S. 2006. Enhanced activity and stability of α-amylase immobilized on alumina. Catal. Commun. 7: 460-465.
    CrossRef
  41. Sheldon RA. 2007. Enzyme immobilization: the quest for optimum performance. Adv. Synth. Catal. 349: 1289-1307.
    CrossRef
  42. 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.
    CrossRef
  43. 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.
    CrossRef
  44. Wefers K, Misra C. 1987. Oxides and hydroxides of aluminum. Technical Paper No. 19. Alcoa Laboratories, Pittsburgh, PA.
  45. Wohlgemuth R. 2010. Asymmetric biocatalysis with microbial enzymes and cells. Curr. Opin. Microbiol. 13: 283-292.
    Pubmed CrossRef
  46. 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.
    Pubmed CrossRef
  47. 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.
    CrossRef
  48. 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.
    Pubmed CrossRef