Characterization of a novel Aspergillus niger beta-glucosidase tolerant to saccharification of lignocellulosic biomass products and fermentation inhibitors
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Alesandra Oriente
Abstract
Properties of beta-glucosidase produced by Aspergillus niger URM 6642 recently isolated from the Atlantic rainforest biome and its potential tolerance to saccharification of lignocellulosic biomass products and fermentation inhibitors was evaluated. The fungus was cultivated under solid state culture conditions at 37°C with different agro-industrial wastes. High levels of beta-glucosidase (3778.9 U g−1) from A. niger were obtained with rice meal as substrate under solid state culture conditions after ten days. Optimum pH for this particular beta-glucosidase activity was 4.0 although it was stable in the range of 4.0 to 7.0. The half-life (T1/2) of beta-glucosidase at 55°C is 3 h. However, at the optimum temperature of the enzyme, 65°C, T1/2 is 20 min. The enzyme showed tolerance to various compounds such as glucose, xylose, 5-hydroxymethyl furfural, furfural, coumarin, ethanol and acetic acid. Therefore, beta-glucosidase from the novel A. niger species may be of potential use in the saccharification of lignocellulosic biomass, as well as an additional enzyme supplement in cellulase cocktails used to increase the yield of fermentable sugars.
References
Gao, Z. Q., Van Hop, D., Yen, L. T., Ando, K., Hiyamuta, S., & Kondo, R. (2012). The production of β-glucosidases by Fusarium proliferatum NBRC109045 isolated from Vietnamese forest. AMB Express, 2, 49. DOI: 10.1186/2191-0855-2-49.10.1186/2191-0855-2-49Search in Google Scholar PubMed PubMed Central
Gao, L., Gao, F., Zhang, D. Y., Zhang, C., Wu, G. H., & Chen, S. L. (2013). Purification and characterization of a new β-glucosidase from Penicillium piceum and its application in enzymatic degradation of delignified corn stover. Bioresource Technology, 147, 658-661. DOI: 10.1016/j.biortech.2013.08.089.10.1016/j.biortech.2013.08.089Search in Google Scholar PubMed
Harnicharnchai, P., Champreda, V., Sornlake, W., & Eurwilaichitr, L. (2009). A thermotolerant β-glucosidase isolated from an endophytic fungi, Periconia sp., with a possible use for biomass conversion to sugars. Protein Expression and Purification, 67, 61-69. DOI: 10.1016/j.pep.2008.05.022.10.1016/j.pep.2008.05.022Search in Google Scholar PubMed
Jørgensen, H., Vibe-Pedersen, J., Larsen, J., & Felby, C. (2007). Liquefaction of lignocellulose at high-solids concentrations. Biotechnology and Bioengineering, 96, 862-870. DOI: 10.1002/bit.21115.10.1002/bit.21115Search in Google Scholar PubMed
Kaushal, R., Sharma, N., & Tandon, D. (2012). Cellulase and xylanase production by co-culture of Aspergillus niger and Fusarium oxysporum utilizing forest waste. Turkish Journal of Biochemistry, 37, 35-41. DOI: 10.5505/tjb.2012.43434.10.5505/tjb.2012.43434Search in Google Scholar
Kaur, J., Chadha, B. S., Kumar, B. A., Kaur, G. S., & Saini, H. S. (2007). Purification and characterization of β-glucosidase from Melanocarpus sp. MTCC 3922. Electronic Journal of Biotechnology, 10(2), 4. DOI: 10.2225/vol10-issue2-fulltext-4.10.2225/vol10-issue2-fulltext-4Search in Google Scholar
Liu, D. Y., Zhang, R. F., Yang, X. M., Zhang, Z. H., Song, S., Miao, S. Z., & Shen, Q. R. (2012). Characterization of a thermostable β-glucosidase from Aspergillus fumigatus Z5, and its functional expression in Pichia pastoris X33. Microbial Cell Factory, 17, 11-25. DOI: 10.1186/1475-2859-11-25.10.1186/1475-2859-11-25Search in Google Scholar PubMed PubMed Central
Ma, S. J., Leng, B., Xu, X. Q., Zhu, X. Z., Shi, Y., Tao, Y. M., Chen, S. X., Long, M. N., & Chen, Q. X. (2011). Purification and characterization of β-1,4-glucosidase from Aspergillus glaucus. African Journal of Biotechnology, 10, 19607-19614. DOI: 10.5897/ajb11.2144.10.5897/AJB11.2144Search in Google Scholar
Masui, D. C., Zimbardi, A. L. R. L., Souza, F. H.M., Guimarães, L. H. S., Furriel, R. P. M., & Jorge, J. A. (2012). Production of a xylose-stimulated β-glucosidase and a cellulase free thermostable xylanase by the thermophilic fungus Humicola brevis var. thermoidea under solid state fermentation. World Journal Microbiology & Biotechnology, 28, 2689-2701. DOI: 10.1007/s11274-012-1079-1.10.1007/s11274-012-1079-1Search in Google Scholar PubMed
Michelin, M. (2013). Aplication of lignocelulosic residues in the production of cellulase and hemicellulase from fungi. In T. Mahendra, & M. L. T. M. Polizelli (Eds.), Fungal enzymes (pp. 32-59). Boca Raton, FL, USA: Taylor & Francis.Search in Google Scholar
Miller, G. L. (1959). Use of dinitrosalicilic acid reagent for determination of reducing sugar. Analytical Chemistry, 31, 426-428. DOI: 10.1021/ac60147a030.10.1021/ac60147a030Search in Google Scholar
Nascimento, C. V., Souza, F. H. M., Masui, D. C., Leone, F. A., Peralta, R.M., Jorge, J. A., & Furriel, R. P. M. (2010). Purification and biochemical properties of a glucose-stimulated β-D-glucosidase produced by Humicola grisea var. thermoidea grown on sugarcane bagasse. Journal of Microbiology, 48, 53-62. DOI: 10.1007/s12275-009-0159-x.10.1007/s12275-009-0159-xSearch in Google Scholar PubMed
Ng, S., Li, C. W., Chan, S. P., Chir, J. L., Chen, P. T., Tong, C. C., Yu, S. M., & Ho, T. H. D. (2010). High-level production of a thermoacidophilic β-glucosidase from Penicillium citrinum YS40-5 by solid-state fermentation with rice bran. Bioresource Technology, 101, 1310-1317. DOI: 10.1016/j.biortech.2009.08.049.10.1016/j.biortech.2009.08.049Search in Google Scholar PubMed
Olofsson, K., Bertilsson, M., & Lidén, G. (2008). A short review on SSF - an interesting process option for ethanol production from lignocellulosic feedstocks. Biotechnology for Biofuels, 1, 1-14. DOI: 10.1186/1754-6834-1-7.10.1186/1754-6834-1-7Search in Google Scholar PubMed PubMed Central
Pei, X. Q., Yi, Z. L., Tang, C. G., & Wu, Z. L. (2011). Three amino acid changes contribute markedly to the thermostability of β-glucosidase BglC from Thermobifida fusca. Bioresource Technology, 102, 3337-3342. DOI: 10.1016/j.biortech.2010.11.025.10.1016/j.biortech.2010.11.025Search in Google Scholar PubMed
Philippoussis, A., Zervakis, G., & Diamantopoulou, P. (2001). Bioconversion of agricultural lignocelulosic wastes through the cultivation of the edible mushrooms Agrocibes aegerita, Volvariella volvacea and Pleurotus spp. World Journal Microbiology & Biotechnology, 17, 191-200. DOI: 10.1023/a:1016685530312.10.1023/A:1016685530312Search in Google Scholar
Qi, B., Wang, L. M., & Liu, X. J. (2009). Purification and characterization of β glucosidase from newly isolated Aspergillus sp. MT-0204. African Journal of Biotechnology, 8, 2367-2374.Search in Google Scholar
Ragauskas, A. J., Williams, C. K., Davison, B. H., Britovsek, G., Cairney, J., Eckert, C. A., Frederick, W. J., Jr., Hallett, J. P., Leak, D. J., Liotta, C. L., Mielenz, J. R., Murphy, R., Templer, R., & Tschaplinski, T. (2006). The path forward for biofuels and biomaterials. Science, 311, 484-489. DOI: 10.1126/science.1114736.10.1126/science.1114736Search in Google Scholar PubMed
Rajoka, M. I., Akhtar, M. W., Hanif, A., & Khalid, A. M. (2006). Production and characterization of a highly active cellobiase from Aspergillus niger grown in solid state fermentation. World Journal of Microbiology & Biotechnology, 22, 991-998. DOI 10.1007/s11274-006-9146-0.10.1007/s11274-006-9146-0Search in Google Scholar
Ribeiro, L. F. C., Ribeiro, L. F., Jorge, J. A., & Polizeli, M. L. T. M. (2014). Screening of filamentous fungi for xylanases and cellulases not inhibited by xylose and glucose. British Biotechnology Journal, 4, 30-39. DOI: 10.9734/bbj/2014/6066.10.9734/BBJ/2014/6066Search in Google Scholar
Singhania, R. R., Sukumaran, R. K., Patel, A. K., Larroche, C., & Pandey, A. (2010). Advancement and comparative profiles in the production technologies using solidstate and submerged fermentation for microbial cellulases. Enzyme and Microbiology Technology, 46, 541-549. DOI: 10.1016/j.enzmictec.2010.03.010.10.1016/j.enzmictec.2010.03.010Search in Google Scholar
Soni, R., Nazir, A., & Chadha, B. S. (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. Industrial Crops and Products, 31, 277-283. DOI: 10.1016/j.indcrop.2009.11.007.10.1016/j.indcrop.2009.11.007Search in Google Scholar
Sonia, K. G., Chadha, E. B. S., Badhan, E. A. K., Saini, H. S., & Bhat, E. M. (2008). Identification of glucose tolerant acid active β-glucosidases from thermophilic and thermotolerant fungi. World Journal Microbiology & Biotechnology, 24, 599-604. DOI: 10.1007/s11274-007-9512-6.10.1007/s11274-007-9512-6Search in Google Scholar
Sørensen, A., Ahring, B. K, Lübeck, M., Ubhayasekera, W., Bruno, K. S., Culley, D. E., & Lübeck, P. S. (2012). Identifying and characterizing the most significant β-glucosidase of the novel species Aspergillus saccharolyticus. Canadian Journal of Microbiology, 58, 1035-1046. DOI: 10.1139/w2012-076.10.1139/w2012-076Search in Google Scholar PubMed
Souza, F. H. M., Nascimento, C. V., Rosa, J. C., Masui, D. C., Leone, F. A., Jorge, J. A., & Furriel, R. P. M. (2010). Purification and biochemical characterization of a mycelial glucose and xylose stimulated β-glucosidase from the thermophilic fungus Humicola insolens. Process Biochemistry, 45, 272-278. DOI: 10.1016/j.procbio.2009.09.018.10.1016/j.procbio.2009.09.018Search in Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725-2729. DOI: 10.1093/molbev/mst197.10.1093/molbev/mst197Search in Google Scholar PubMed PubMed Central
Tengborg, C., Galbe, M., & Zacchi, G. (2001). Influence of enzyme loading and physical parameters on the enzymatic hydrolysis of steam pretreated softwood. Biotechnology Progress, 17, 110-117. DOI: 10.1021/bp000145+.10.1021/bp000145+Search in Google Scholar PubMed
Tu, M. B., Zhang, X., Kurabi, A., Gilkes, N., Mabee,W., & Saddler, J. (2006). Immobilization of β-glucosidase on Eupergit C for lignocelluloses hydrolysis. Biotechnology Letters, 28, 151-156. DOI: 10.1007/s10529-005-5328-3.10.1007/s10529-005-5328-3Search in Google Scholar PubMed
Turenne, C. Y., Sanche, S. E., Hoban, D. J., Karlowsky, J. A., & Kabani, A. M. (1999). Rapid identification of fungi by using the ITS2 genetic region and an automated fluorescent capillary electrophoresis system. Journal of Clinical Microbiology, 7, 1846-1851.10.1128/JCM.37.6.1846-1851.1999Search in Google Scholar PubMed PubMed Central
Vintila, T., Dragomirescu, M., Croitoriu, V., Vintila, C., Barbu, H., & Sand, C. (2010). Saccharification of lignocelluloses - with reference to Miscanthus - using different cellulases. Romanian Biotechnological Letters, 15, 5498-5504.Search in Google Scholar
White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR Protocols: a guide to methods and applications (pp. 315-322). New York, NY, USA: Academic Press.Search in Google Scholar
Wu, Z., & Lee, Y. Y. (1997). Inhibition of the enzymatic hydrolysis of cellulose by ethanol. Biotechnology Letters, 19, 977-979. DOI: 10.1023/a:1018487015129.10.1023/A:1018487015129Search in Google Scholar
Yang, S. Q., Jiang, Z. Q., Yan, Q. J., & Zhu, H. F. (2008). Characterization of a thermostable extracellular β-glucosidase with activities of exoglucanase and transglycosylation from Paecilomyces thermophila. Journal of Agricultural and Food Chemistry, 56, 602-608. DOI: 10.1021/jf072279.10.1021/jf072279+Search in Google Scholar PubMed
Zanoelo, F. F., Polizeli, M. L. T. M., Terenzi, H. F., & Jorge, J. A. (2004). β-Glucosidase activity from the thermophilic fungus Scytalidium thermophilum is stimulated by glucose and xylose. FEMS Microbiology Letters, 240, 137-143. DOI: 10.1016/j.femsle.2004.09.021. 10.1016/j.femsle.2004.09.021Search in Google Scholar PubMed
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- Integrated investigations for the characterisation of Roman lead-glazed pottery from Pompeii and Herculaneum (Italy)
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