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References

  1. Badhan AK, Chadha BS, Kaur J, Saini HS, Bhat MK. 2007. Production of multiple xylanolytic and cellulolytic enzymes by thermophilic fungus Myceliophthora sp. IMI 387099. Bioresour. Technol. 98: 504-510.
    Pubmed CrossRef
  2. Bagga PS, Sandhu DK, Sharma S. 1990. Purification and characterization of cellulolytic enzymes produced by Aspergillus nidulans. J. Appl. Bacteriol. 68: 61-68.
    Pubmed CrossRef
  3. Bansal N, Tewari R, Soni R, Soni SK. 2012. Production of cellulases from Aspergillus niger NS-2 in solid state fermentation on agricultural and kitchen waste residues. Waste Manag. 32:1341-1346.
    Pubmed CrossRef
  4. Bischoff K, Wicklow D, Jordan D, Rezende S, Liu S, Hughes S, Rich J. 2009. Extracellular hemicellulolytic enzymes from the maize endophyte Acremonium zeae. Curr. Microbiol. 58:499-503.
    Pubmed CrossRef
  5. Chapla D, Divecha J, Madamwar D, Shah A. 2010. Utilization of agro-industrial waste for xylanase production by Aspergillus foetidus MTCC 4898 under solid state fermentation and its application in saccharification. Biochem. Eng. J. 49: 361-369.
    CrossRef
  6. Cherubini F. 2010. The biorefinery concept: using biomass instead of oil for producing energy and chemicals. Energy Conver. Manag. 51: 1412-1421.
    CrossRef
  7. Delabona PdS, Pirota RDPB, Codima CA, Tremacoldi CR, Rodrigues A, Farinas CS. 2013. Effect of initial moisture content on two Amazon rainforest Aspergillus strains cultivated on agro-industrial residues: biomass-degrading enzymes production and characterization. Ind. Crops Prod. 42: 236242.
    CrossRef
  8. Falkoski DL, Guimarães VM, de Almeida MN, Alfenas AC, Colodette JL, de Rezende ST. 2013. Chrysoporthe cubensis: a new source of cellulases and hemicellulases to application in biomass saccharification processes. Bioresour. Technol. 130:296-305.
    Pubmed CrossRef
  9. Fernández-Espinar M, Piñaga F, de Graaff L, Visser J, Ramón D, Vallés S. 1994. Purification, characterization and regulation of the synthesis of an Aspergillus nidulans acidic xylanase. Appl. Microbiol. Biotechnol. 42: 555-562.
    CrossRef
  10. Gao J, Weng H, Zhu D, Yuan M, Guan F, Xi Y. 2008. Production and characterization of cellulolytic enzymes from the thermoacidophilic fungal Aspergillus terreus M11 under solid-state cultivation of corn stover. Bioresour. Technol. 99: 7623-7629.
    Pubmed CrossRef
  11. Ghose TK. 1987. Measurement of cellulase activities. Pure Appl. Chem. 59: 257–268.
    CrossRef
  12. Gusakov AV. 2011. Alternatives to Trichoderma reesei in biofuel production. Trends Biotechnol. 29: 419-425.
    Pubmed CrossRef
  13. Herculano P, Porto T, Moreira K, Pinto GS, Souza-Motta C, Porto A. 2011. Cellulase production by Aspergillus japonicus URM5620 using waste from castor bean (Ricinus communis L.) under solid-state fermentation. Appl. Biochem. Biotechnol. 165:1057-1067.
    Pubmed CrossRef
  14. Hölker U, Höfer M, Lenz J. 2004. Biotechnological advantages of laboratory-scale solid-state fermentation with fungi. Appl. Microbiol. Biotechnol. 64: 175-186.
    Pubmed CrossRef
  15. Jatinder K, Chadha BS, Saini HS. 2006. Optimization of medium components for production of cellulases by Melanocarpus sp. MTCC 3922 under solid-state fermentation. World J. Microbiol. Biotechnol. 22: 15-22.
    CrossRef
  16. Kachlishvili E, Penninckx M, Tsiklauri N, Elisashvili V. 2006. Effect of nitrogen source on lignocellulolytic enzyme production by white-rot basidiomycetes under solid-state cultivation. World J. Microbiol. Biotechnol. 22: 391-397.
    CrossRef
  17. Kumar P, Barrett DM, Delwiche MJ, Stroeve P. 2009. Methods for pretreatment of lignocellulosic biomass for efficient hydrolysis and biofuel production. Ind. Eng. Chem. Res. 48: 3713-3729.
    CrossRef
  18. Kumar R, Singh S, Singh O. 2008. Bioconversion of lignocellulosic biomass: biochemical and molecular perspectives. J. Ind. Microbiol. Biotechnol. 35: 377-391.
    Pubmed CrossRef
  19. Kwon K-S, Lee J, Kang HG, Hah YC. 1994. Detection of βglucosidase activity in polyacrylamide gels with esculin as substrate. Appl. Environ. Microbiol. 60: 4584-4586.
    Pubmed
  20. Liu G, Qin Y, Li Z, Qu Y. 2013. Development of highly efficient, low-cost lignocellulolytic enzyme systems in the post-genomic era. Biotechnol. Adv. 31: 962-975.
    Pubmed CrossRef
  21. Miller GL, Blum R, Glennon WE, Burton AL. 1960. Measurement of carboxymethylcellulase activity. Anal. Biochem. 1: 127-132.
    CrossRef
  22. Narra M, Dixit G, Divecha J, Madamwar D, Shah AR. 2012. Production of cellulases by solid state fermentation with Aspergillus terreus and enzymatic hydrolysis of mild alkalitreated rice straw. Bioresour. Technol. 121: 355-361.
    Pubmed CrossRef
  23. Nazir A , Soni R , Saini HS, Kaur A , Chadha B S. 2 010. Profiling differential expression of cellulases and metabolite footprints in Aspergillus terreus. Appl. Biochem. Biotechnol. 162: 538-547.
    Pubmed CrossRef
  24. Noratiqah K, Madihah MS, Aisyah BS, Eva MS, Suraini AA, Kamarulzaman K. 2013. Statistical optimization of enzymatic degradation process for oil palm empty fruit bunch (OPEFB) in rotary drum bioreactor using crude cellulase produced from Aspergillus niger EFB1. Biochem. Eng. J. 75: 8-20.
    CrossRef
  25. Pandey ALC, Soccol CR. 2001. General consideration about solid-state fermentation process, pp. 13-25. In Pandey A (ed.). Solid State Fermentation in Biotechnology: Fundamentals and Applications. Asiatech Publishers Inc., New Delhi.
    Pubmed
  26. Pardo A. 1996. Effect of surfactants on cellulase production by Nectria catalinensis. Curr. Microbiol. 33: 275-278.
    Pubmed CrossRef
  27. Qing Q, Wyman C. 2011. Supplementation with xylanase and beta-xylosidase to reduce xylo-oligomer and xylan inhibition of enzymatic hydrolysis of cellulose and pretreated corn stover. Biotechnol. Biofuels 4: 18.
    Pubmed CrossRef
  28. Qing Q, Yang B, Wyman CE. 2010. Xylooligomers are strong inhibitors of cellulose hydrolysis by enzymes. Bioresour. Technol. 101: 9624-9630.
    Pubmed CrossRef
  29. Rattanachomsri U, Tanapongpipat S, Eurwilaichitr L, Champreda V. 2009. Simultaneous non-thermal saccharification of cassava pulp by multi-enzyme activity and ethanol fermentation by Candida tropicalis. J. Biosci. Bioeng. 107: 488-493.
    Pubmed CrossRef
  30. Soni R, Nazir A, Chadha BS. 2010. Optimization of cellulase production by a versatile Aspergillus fumigatus fresenius strain (AMA) capable of efficient deinking and enzymatic hydrolysis of Solka Floc and bagasse. Ind. Crops Products 31:277-283.
    CrossRef
  31. Suwannarangsee S, Bunterngsook B, Arnthong J, Paemanee A, Thamchaipenet A, Eurwilaichitr L, et al. 2012. Optimisation of synergistic biomass-degrading enzyme systems for efficient rice straw hydrolysis using an experimental mixture design. Bioresour. Technol. 119: 252-261.
    Pubmed CrossRef
  32. Van Dyk JS, Pletschke BI. 2012. A review of lignocellulose bioconversion using enzymatic hydrolysis and synergistic cooperation between enzymes — Factors affecting enzymes, conversion and synergy. Biotechnol. Adv. 30: 1458-1480.
    Pubmed CrossRef
  33. Walker LP, Wilson DB. 1991. Enzymatic hydrolysis of cellulose: an overview. Bioresour. Technol. 36: 3-14.
    CrossRef
  34. Wen Z, Liao W, Chen S. 2005. Production of cellulase/βglucosidase by the mixed fungi culture of Trichoderma reesei and Aspergillus phoenicis on dairy manure, pp. 93-104. In Davison B, Evans B, Finkelstein M, McMillan J (eds.). Twenty-Sixth Symposium on Biotechnology for Fuels and Chemicals. Humana Press.
  35. Zaldívar M, Velásquez JC, Contreras I, Pérez LM. 2001. Trichoderma aureoviride 7-121, a mutant with enhanced production of lytic enzymes: its potential use in waste cellulose degradation and/or biocontrol. Electron. J. Biotechnol. DOI:10.2225/vol4-issue3-fulltex-7.

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Article

Research article

J. Microbiol. Biotechnol. 2014; 24(10): 1427-1437

Published online October 28, 2014 https://doi.org/10.4014/jmb.1406.06050

Copyright © The Korean Society for Microbiology and Biotechnology.

Production and Characterization of Multi-Polysaccharide Degrading Enzymes from Aspergillus aculeatus BCC199 for Saccharification of Agricultural Residues

Surisa Suwannarangsee 1*, Jantima Arnthong 1, Lily Eurwilaichitr 1 and Verawat Champreda 1

Enzyme Technology Laboratory, Bioresources Technology Unit, National Center for Genetic Engineering and Biotechnology, Klong Luang, Pathumthani 12120, Thailand

Received: June 17, 2014; Accepted: July 3, 2014

Abstract

Enzymatic hydrolysis of lignocellulosic biomass into fermentable sugars is a key step in the
conversion of agricultural by-products to biofuels and value-added chemicals. Utilization of a
robust microorganism for on-site production of biomass-degrading enzymes has gained
increasing interest as an economical approach for supplying enzymes to biorefinery processes.
In this study, production of multi-polysaccharide-degrading enzymes from Aspergillus
aculeatus BCC199 by solid-state fermentation was improved through the statistical design
approach. Among the operational parameters, yeast extract and soybean meal as well as the
nonionic surfactant Tween 20 and initial pH were found as key parameters for maximizing
production of cellulolytic and hemicellulolytic enzymes. Under the optimized condition, the
production of FPase, endoglucanase, β-glucosidase, xylanase, and β-xylosidase was achieved
at 23, 663, 88, 1,633, and 90 units/g of dry substrate, respectively. The multi-enzyme extract
was highly efficient in the saccharification of alkaline-pretreated rice straw, corn cob, and corn
stover. In comparison with commercial cellulase preparations, the BCC199 enzyme mixture
was able to produce remarkable yields of glucose and xylose, as it contained higher relative
activities of β-glucosidase and core hemicellulases (xylanase and β-xylosidase). These results
suggested that the crude enzyme extract from A. aculeatus BCC199 possesses balanced
cellulolytic and xylanolytic activities required for the efficient saccharification of lignocellulosic
biomass feedstocks, and supplementation of external β-glucosidase or xylanase was dispensable.
The work thus demonstrates the high potential of A. aculeatus BCC199 as a promising
producer of lignocellulose-degrading enzymes for the biomass conversion industry.

Keywords: Biomass saccharification, Cellulase, Hemicellulase, Solid-state fermentation, Response surface methodology, Biorefinery

References

  1. Badhan AK, Chadha BS, Kaur J, Saini HS, Bhat MK. 2007. Production of multiple xylanolytic and cellulolytic enzymes by thermophilic fungus Myceliophthora sp. IMI 387099. Bioresour. Technol. 98: 504-510.
    Pubmed CrossRef
  2. Bagga PS, Sandhu DK, Sharma S. 1990. Purification and characterization of cellulolytic enzymes produced by Aspergillus nidulans. J. Appl. Bacteriol. 68: 61-68.
    Pubmed CrossRef
  3. Bansal N, Tewari R, Soni R, Soni SK. 2012. Production of cellulases from Aspergillus niger NS-2 in solid state fermentation on agricultural and kitchen waste residues. Waste Manag. 32:1341-1346.
    Pubmed CrossRef
  4. Bischoff K, Wicklow D, Jordan D, Rezende S, Liu S, Hughes S, Rich J. 2009. Extracellular hemicellulolytic enzymes from the maize endophyte Acremonium zeae. Curr. Microbiol. 58:499-503.
    Pubmed CrossRef
  5. Chapla D, Divecha J, Madamwar D, Shah A. 2010. Utilization of agro-industrial waste for xylanase production by Aspergillus foetidus MTCC 4898 under solid state fermentation and its application in saccharification. Biochem. Eng. J. 49: 361-369.
    CrossRef
  6. Cherubini F. 2010. The biorefinery concept: using biomass instead of oil for producing energy and chemicals. Energy Conver. Manag. 51: 1412-1421.
    CrossRef
  7. Delabona PdS, Pirota RDPB, Codima CA, Tremacoldi CR, Rodrigues A, Farinas CS. 2013. Effect of initial moisture content on two Amazon rainforest Aspergillus strains cultivated on agro-industrial residues: biomass-degrading enzymes production and characterization. Ind. Crops Prod. 42: 236242.
    CrossRef
  8. Falkoski DL, Guimarães VM, de Almeida MN, Alfenas AC, Colodette JL, de Rezende ST. 2013. Chrysoporthe cubensis: a new source of cellulases and hemicellulases to application in biomass saccharification processes. Bioresour. Technol. 130:296-305.
    Pubmed CrossRef
  9. Fernández-Espinar M, Piñaga F, de Graaff L, Visser J, Ramón D, Vallés S. 1994. Purification, characterization and regulation of the synthesis of an Aspergillus nidulans acidic xylanase. Appl. Microbiol. Biotechnol. 42: 555-562.
    CrossRef
  10. Gao J, Weng H, Zhu D, Yuan M, Guan F, Xi Y. 2008. Production and characterization of cellulolytic enzymes from the thermoacidophilic fungal Aspergillus terreus M11 under solid-state cultivation of corn stover. Bioresour. Technol. 99: 7623-7629.
    Pubmed CrossRef
  11. Ghose TK. 1987. Measurement of cellulase activities. Pure Appl. Chem. 59: 257–268.
    CrossRef
  12. Gusakov AV. 2011. Alternatives to Trichoderma reesei in biofuel production. Trends Biotechnol. 29: 419-425.
    Pubmed CrossRef
  13. Herculano P, Porto T, Moreira K, Pinto GS, Souza-Motta C, Porto A. 2011. Cellulase production by Aspergillus japonicus URM5620 using waste from castor bean (Ricinus communis L.) under solid-state fermentation. Appl. Biochem. Biotechnol. 165:1057-1067.
    Pubmed CrossRef
  14. Hölker U, Höfer M, Lenz J. 2004. Biotechnological advantages of laboratory-scale solid-state fermentation with fungi. Appl. Microbiol. Biotechnol. 64: 175-186.
    Pubmed CrossRef
  15. Jatinder K, Chadha BS, Saini HS. 2006. Optimization of medium components for production of cellulases by Melanocarpus sp. MTCC 3922 under solid-state fermentation. World J. Microbiol. Biotechnol. 22: 15-22.
    CrossRef
  16. Kachlishvili E, Penninckx M, Tsiklauri N, Elisashvili V. 2006. Effect of nitrogen source on lignocellulolytic enzyme production by white-rot basidiomycetes under solid-state cultivation. World J. Microbiol. Biotechnol. 22: 391-397.
    CrossRef
  17. Kumar P, Barrett DM, Delwiche MJ, Stroeve P. 2009. Methods for pretreatment of lignocellulosic biomass for efficient hydrolysis and biofuel production. Ind. Eng. Chem. Res. 48: 3713-3729.
    CrossRef
  18. Kumar R, Singh S, Singh O. 2008. Bioconversion of lignocellulosic biomass: biochemical and molecular perspectives. J. Ind. Microbiol. Biotechnol. 35: 377-391.
    Pubmed CrossRef
  19. Kwon K-S, Lee J, Kang HG, Hah YC. 1994. Detection of βglucosidase activity in polyacrylamide gels with esculin as substrate. Appl. Environ. Microbiol. 60: 4584-4586.
    Pubmed
  20. Liu G, Qin Y, Li Z, Qu Y. 2013. Development of highly efficient, low-cost lignocellulolytic enzyme systems in the post-genomic era. Biotechnol. Adv. 31: 962-975.
    Pubmed CrossRef
  21. Miller GL, Blum R, Glennon WE, Burton AL. 1960. Measurement of carboxymethylcellulase activity. Anal. Biochem. 1: 127-132.
    CrossRef
  22. Narra M, Dixit G, Divecha J, Madamwar D, Shah AR. 2012. Production of cellulases by solid state fermentation with Aspergillus terreus and enzymatic hydrolysis of mild alkalitreated rice straw. Bioresour. Technol. 121: 355-361.
    Pubmed CrossRef
  23. Nazir A , Soni R , Saini HS, Kaur A , Chadha B S. 2 010. Profiling differential expression of cellulases and metabolite footprints in Aspergillus terreus. Appl. Biochem. Biotechnol. 162: 538-547.
    Pubmed CrossRef
  24. Noratiqah K, Madihah MS, Aisyah BS, Eva MS, Suraini AA, Kamarulzaman K. 2013. Statistical optimization of enzymatic degradation process for oil palm empty fruit bunch (OPEFB) in rotary drum bioreactor using crude cellulase produced from Aspergillus niger EFB1. Biochem. Eng. J. 75: 8-20.
    CrossRef
  25. Pandey ALC, Soccol CR. 2001. General consideration about solid-state fermentation process, pp. 13-25. In Pandey A (ed.). Solid State Fermentation in Biotechnology: Fundamentals and Applications. Asiatech Publishers Inc., New Delhi.
    Pubmed
  26. Pardo A. 1996. Effect of surfactants on cellulase production by Nectria catalinensis. Curr. Microbiol. 33: 275-278.
    Pubmed CrossRef
  27. Qing Q, Wyman C. 2011. Supplementation with xylanase and beta-xylosidase to reduce xylo-oligomer and xylan inhibition of enzymatic hydrolysis of cellulose and pretreated corn stover. Biotechnol. Biofuels 4: 18.
    Pubmed CrossRef
  28. Qing Q, Yang B, Wyman CE. 2010. Xylooligomers are strong inhibitors of cellulose hydrolysis by enzymes. Bioresour. Technol. 101: 9624-9630.
    Pubmed CrossRef
  29. Rattanachomsri U, Tanapongpipat S, Eurwilaichitr L, Champreda V. 2009. Simultaneous non-thermal saccharification of cassava pulp by multi-enzyme activity and ethanol fermentation by Candida tropicalis. J. Biosci. Bioeng. 107: 488-493.
    Pubmed CrossRef
  30. Soni R, Nazir A, Chadha BS. 2010. Optimization of cellulase production by a versatile Aspergillus fumigatus fresenius strain (AMA) capable of efficient deinking and enzymatic hydrolysis of Solka Floc and bagasse. Ind. Crops Products 31:277-283.
    CrossRef
  31. Suwannarangsee S, Bunterngsook B, Arnthong J, Paemanee A, Thamchaipenet A, Eurwilaichitr L, et al. 2012. Optimisation of synergistic biomass-degrading enzyme systems for efficient rice straw hydrolysis using an experimental mixture design. Bioresour. Technol. 119: 252-261.
    Pubmed CrossRef
  32. Van Dyk JS, Pletschke BI. 2012. A review of lignocellulose bioconversion using enzymatic hydrolysis and synergistic cooperation between enzymes — Factors affecting enzymes, conversion and synergy. Biotechnol. Adv. 30: 1458-1480.
    Pubmed CrossRef
  33. Walker LP, Wilson DB. 1991. Enzymatic hydrolysis of cellulose: an overview. Bioresour. Technol. 36: 3-14.
    CrossRef
  34. Wen Z, Liao W, Chen S. 2005. Production of cellulase/βglucosidase by the mixed fungi culture of Trichoderma reesei and Aspergillus phoenicis on dairy manure, pp. 93-104. In Davison B, Evans B, Finkelstein M, McMillan J (eds.). Twenty-Sixth Symposium on Biotechnology for Fuels and Chemicals. Humana Press.
  35. Zaldívar M, Velásquez JC, Contreras I, Pérez LM. 2001. Trichoderma aureoviride 7-121, a mutant with enhanced production of lytic enzymes: its potential use in waste cellulose degradation and/or biocontrol. Electron. J. Biotechnol. DOI:10.2225/vol4-issue3-fulltex-7.