A Highly Glucose Tolerant ß-Glucosidase from Malbranchea pulchella (MpBg3) Enables Cellulose Saccharification.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
24 04 2020
24 04 2020
Historique:
received:
10
09
2019
accepted:
13
03
2020
entrez:
26
4
2020
pubmed:
26
4
2020
medline:
22
12
2020
Statut:
epublish
Résumé
β-glucosidases catalyze the hydrolysis β-1,4, β-1,3 and β-1,6 glucosidic linkages from non-reducing end of short chain oligosaccharides, alkyl and aryl β-D-glucosides and disaccharides. They catalyze the rate-limiting reaction in the conversion of cellobiose to glucose in the saccharification of cellulose for second-generation ethanol production, and due to this important role the search for glucose tolerant enzymes is of biochemical and biotechnological importance. In this study we characterize a family 3 glycosyl hydrolase (GH3) β-glucosidase (Bgl) produced by Malbranchea pulchella (MpBgl3) grown on cellobiose as the sole carbon source. Kinetic characterization revealed that the MpBgl3 was highly tolerant to glucose, which is in contrast to many Bgls that are completely inhibited by glucose. A 3D model of MpBgl3 was generated by molecular modeling and used for the evaluation of structural differences with a Bgl3 that is inhibited by glucose. Taken together, our results provide new clues to understand the glucose tolerance in GH3 β-glucosidases.
Identifiants
pubmed: 32332833
doi: 10.1038/s41598-020-63972-y
pii: 10.1038/s41598-020-63972-y
pmc: PMC7181827
doi:
Substances chimiques
Cellobiose
16462-44-5
Carbon
7440-44-0
Cellulose
9004-34-6
beta-Glucosidase
EC 3.2.1.21
Glucose
IY9XDZ35W2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
6998Références
Bhatia, Y., Mishra, S. & Bisaria, V. S. Microbial beta-glucosidases: Cloning, properties, and applications. Crit. Rev. Biotechnol. 22, 375–407, https://doi.org/10.1080/07388550290789568 (2002).
doi: 10.1080/07388550290789568
pubmed: 12487426
Bai, H. Z. et al. Production, purification and characterization of novel beta glucosidase from newly isolated Penicillium simplicissimum H-11 in submerged fermentation. Excli J 12, 528–540 (2013).
pubmed: 26609283
pmcid: 4657531
Sorensen, A., Lubeck, M., Lubeck, P. S. & Ahring, B. K. Fungal beta-glucosidases: a bottleneck in industrial use of lignocellulosic materials. Biomolecules 3, 612–631, https://doi.org/10.3390/biom3030612 (2013).
doi: 10.3390/biom3030612
pubmed: 24970184
pmcid: 4030957
Mallerman, J., Papinutti, L. & Levin, L. Characterization of beta-glucosidase produced by the white rot fungus Flammulina velutipes. J. Microbiol. Biotechnol. 25, 57–65, https://doi.org/10.4014/jmb.1401.01045 (2015).
doi: 10.4014/jmb.1401.01045
pubmed: 25189408
Harnpicharnchai, P., Champreda, V., Sornlake, W. & Eurwilaichitr, L. A thermotolerant beta-glucosidase isolated from an endophytic fungi, Periconia sp., with a possible use for biomass conversion to sugars. Protein. Expr. Purif 67, 61–69, https://doi.org/10.1016/j.pep.2008.05.022 (2009).
doi: 10.1016/j.pep.2008.05.022
pubmed: 18602476
Dan, S. et al. Cloning, expression, characterization, and nucleophile identification of family 3, Aspergillus niger beta-glucosidase. J. Biol. Chem. 275, 4973–4980, https://doi.org/10.1074/jbc.275.7.4973 (2000).
doi: 10.1074/jbc.275.7.4973
pubmed: 10671536
Singhania, R. R., Patel, A. K., Sukumaran, R. K., Larroche, C. & Pandey, A. Role and significance of beta-glucosidases in the hydrolysis of cellulose for bioethanol production. Bioresour. Technol. 127, 500–507, https://doi.org/10.1016/j.biortech.2012.09.012 (2013).
doi: 10.1016/j.biortech.2012.09.012
pubmed: 23069613
Asha, B. M., Pathma, J. & Sakthivel, N. Isolation and characterization of a novel thermostable beta-glucosidase from Bacillus subtilis SU40. Prikladnaia biokhimiia i mikrobiologiia 51, 24–29, https://doi.org/10.7868/s0555109915010031 (2015).
doi: 10.7868/s0555109915010031
pubmed: 25842900
Srivastava, N. et al. Microbial beta glucosidase enzymes: recent advances in biomass conversation for biofuels application. Biomolecules 9, https://doi.org/10.3390/biom9060220 (2019).
Wang, Y., Li, J. & Xu, Y. Characterization of novel beta-glucosidases with transglycosylation properties from Trichosporon asahii. J. Agric. Food Chemistry 59, 11219–11227, https://doi.org/10.1021/jf203693v (2011).
doi: 10.1021/jf203693v
Uchiyama, T., Miyazaki, K. & Yaoi, K. Characterization of a novel beta-glucosidase from a compost microbial metagenome with strong transglycosylation activity. J. Biol. Chem. 288, 18325–18334, https://doi.org/10.1074/jbc.M113.471342 (2013).
doi: 10.1074/jbc.M113.471342
pubmed: 23661705
pmcid: 3689974
Salgado, J. C. S., Meleiro, L. P., Carli, S. & Ward, R. J. Glucose tolerant and glucose stimulated beta-glucosidases - A review. Bioresour. Technol. 267, 704–713, https://doi.org/10.1016/j.biortech.2018.07.137 (2018).
doi: 10.1016/j.biortech.2018.07.137
pubmed: 30093225
Zaldívar, M., Velásquez, J. C., Contreras, I. & Pérez, L. M. Trichoderma aureoviride 7-121, a mutant with enhanced production of lytic enzymes: its potential use in waste cellulose degradation and/or biocontrol. Electronic J. Biotechnol. 4, 13–14, https://doi.org/10.2225/vol4-issue3-fulltext-7 (2001).
doi: 10.2225/vol4-issue3-fulltext-7
Zanoelo, F. F., Polizeli, M. L. T. M., Terenzi, H. F. & Jorge, J. A. Beta-glucosidase activity from the thermophilic fungus Scytalidium thermophilum is stimulated by glucose and xylose. FEMS Microbiol. Lett. 240, 137–143, https://doi.org/10.1016/j.femsle.2004.09.021 (2004).
doi: 10.1016/j.femsle.2004.09.021
pubmed: 15522500
Saha, B. C., Freer, S. N. & Bothast, R. J. Production, purification, and properties of a thermostable beta-glucosidase from a color variant strain of Aureobasidium pullulans. Appl. Environ. Microbiol. 60, 3774–3780 (1994).
doi: 10.1128/AEM.60.10.3774-3780.1994
Pereira, M. G. et al. Biochemical properties of an extracellular trehalase from Malbranchea pulchella var. Sulfurea. J. Microbiol. 49, 809–815, https://doi.org/10.1007/s12275-011-0532-4 (2011).
doi: 10.1007/s12275-011-0532-4
pubmed: 22068499
Ribeiro, L. F. C. et al. A novel thermostable xylanase GH10 from Malbranchea pulchella expressed in Aspergillus nidulans with potential applications in biotechnology. Biotechnol. Biofuels 7, 115, https://doi.org/10.1186/1754-6834-7-115 (2014).
doi: 10.1186/1754-6834-7-115
pubmed: 25788980
pmcid: 4364333
Matsuo, M. & Yasui, T. Properties of xylanase of Malbranchea pulchella var sulfurea no-48. Agr. Biol. Chem. Tokyo 49, 839–841, https://doi.org/10.1080/00021369.1985.10866806 (1985).
doi: 10.1080/00021369.1985.10866806
Monteiro, L. M. O. et al. Efficient hydrolysis of wine and grape juice anthocyanins by Malbranchea pulchella beta-glucosidase immobilized on MANAE-agarose and ConA-Sepharose supports. Int. J. Biol. Macromol. 136, 1133–1141, https://doi.org/10.1016/j.ijbiomac.2019.06.106 (2019).
doi: 10.1016/j.ijbiomac.2019.06.106
pubmed: 31220494
Decker, C. H., Visser, J. & Schreier, P. Beta-glucosidases from five black Aspergillus species: study of their physico-chemical and biocatalytic properties. J. Agric. Food Chemistry 48, 4929–4936, https://doi.org/10.1021/jf000434d (2000).
doi: 10.1021/jf000434d
Zhu, F. M., Du, B., Gao, H. S., Liu, C. J. & Li, J. Purification and characterization of an intracellular beta-glucosidase from the protoplast fusant of Aspergillus oryzae and Aspergillus niger. Prikl. Biokhim. Mikrobiol. 46, 678–684 (2010).
pubmed: 21254729
Suzuki, K. et al. Crystal structures of glycoside hydrolase family 3 beta-glucosidase 1 from Aspergillus aculeatus. Biochem. J. 452, 211–221, https://doi.org/10.1042/BJ20130054 (2013).
doi: 10.1042/BJ20130054
pubmed: 23537284
Giuseppe, P. O. et al. Structural basis for glucose tolerance in GH1 beta-glucosidases. Acta Crystallogr. D. 70, 1631–1639, https://doi.org/10.1107/S1399004714006920 (2014).
doi: 10.1107/S1399004714006920
pubmed: 24914974
Kudo, K., Watanabe, A., Ujiie, S., Shintani, T. & Gomi, K. Purification and enzymatic characterization of secretory glycoside hydrolase family 3 (GH3) aryl beta-glucosidases screened from Aspergillus oryzae genome. J. Biosci. Bioeng. 120, 614–623, https://doi.org/10.1016/j.jbiosc.2015.03.019 (2015).
doi: 10.1016/j.jbiosc.2015.03.019
pubmed: 25936960
Xu, Z., Zhang, L. & Yu, P. Optimization of a heat-tolerant beta-glucosidase production by Bacillus sp. ZJ1308 and its purification and characterization. Biotechnol. Appl. Biochem. 63, 553–563, https://doi.org/10.1002/bab.1405 (2016).
doi: 10.1002/bab.1405
pubmed: 26077129
Watanabe, A., Suzuki, M., Ujiie, S. & Gomi, K. Purification and enzymatic characterization of a novel beta-1,6-glucosidase from Aspergillus oryzae. J. Biosci. Bioeng. 121, 259–264, https://doi.org/10.1016/j.jbiosc.2015.07.011 (2016).
doi: 10.1016/j.jbiosc.2015.07.011
pubmed: 26320404
Krajewska, B. Application of chitin- and chitosan-based materials for enzyme immobilizations: a review. Enzyme Microb. Technol. 35, 126–139, https://doi.org/10.1016/j.enzmictec.2003.12.013 (2004).
doi: 10.1016/j.enzmictec.2003.12.013
Rizzatti, A. C., Jorge, J. A., Terenzi, H. F., Rechia, C. G. & Polizeli, M. L. T. M. Purification and properties of a thermostable extracellular beta-D-xylosidase produced by a thermotolerant Aspergillus phoenicis. J. Ind. Microbiol. Biotechnol. 26, 156–160, https://doi.org/10.1038/sj/jim/7000107 (2001).
doi: 10.1038/sj/jim/7000107
pubmed: 11420656
Baffi, M. A. et al. A novel beta-glucosidase from Sporidiobolus pararoseus: characterization and application in winemaking. J. Food Sci. 76, C997–1002, https://doi.org/10.1111/j.1750-3841.2011.02293.x (2011).
doi: 10.1111/j.1750-3841.2011.02293.x
pubmed: 21819399
Joo, A. R. et al. Production and characterization of beta-1,4-glucosidase from a strain of Penicillium pinophilum. Process. Biochem. 45, 851–858, https://doi.org/10.1016/j.procbio.2010.02.005 (2010).
doi: 10.1016/j.procbio.2010.02.005
Zollner, H. Handbook of enzyme inhibitors. (VCH Publishers, 1999).
Cairns, J. R. K. & Esen, A. Beta-Glucosidases. Cell. Mol. Life Sci. 67, 3389–3405, https://doi.org/10.1007/s00018-010-0399-2 (2010).
doi: 10.1007/s00018-010-0399-2
Narasimha, G., Sridevi, A., Ramanjaneyulu, G. & Reddy, B. R. Purification and characterization of beta-glucosidase from Aspergillus niger. Int. J. Food Prop. 19, 652–661, https://doi.org/10.1080/10942912.2015.1023398 (2016).
doi: 10.1080/10942912.2015.1023398
Zhang, Z. et al. Predominance of Trichoderma and Penicillium in cellulolytic aerobic filamentous fungi from subtropical and tropical forests in China, and their use in finding highly efficient beta-glucosidase. Biotechnol. Biofuels 7, Artn 10710.1186/1754-6834-7-107 (2014).
Lin, L. L., Yan, R., Liu, Y. Q. & Jiang, W. J. In-depth investigation of enzymatic hydrolysis of biomass wastes based on three major components: Cellulose, hemicellulose and lignin. Bioresour. Technol. 101, 8217–8223, https://doi.org/10.1016/j.biortech.2010.05.084 (2010).
doi: 10.1016/j.biortech.2010.05.084
pubmed: 20639116
Cooney, D. G. & Emerson, R. Thermophilic fungi: An account of their biology, activities, and classification. (W. H. Freeman, 1964).
Bradford, M. M. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem 72, 248–254, https://doi.org/10.1006/abio.1976.9999 (1976).
doi: 10.1006/abio.1976.9999
pubmed: 942051
Kwon, K. S., Lee, J., Kang, H. G. & Hah, Y. C. Detection of beta-glucosidase activity in polyacrylamide gels with esculin as substrate. Appl. Environ. Microbiol. 60, 4584–4586 (1994).
doi: 10.1128/AEM.60.12.4584-4586.1994
Leone, F. A., Baranauskas, J. A., Furriel, R. P. & Borin, I. A. SigrafW: An easy-to-use program for fitting enzyme kinetic data. Biochemistry and molecular biology education: a bimonthly publication of the International Union of Biochemistry and Molecular Biology 33, 399–403, https://doi.org/10.1002/bmb.2005.49403306399 (2005).
doi: 10.1002/bmb.2005.49403306399
Zhang, Y. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9, 40, https://doi.org/10.1186/1471-2105-9-40 (2008).
doi: 10.1186/1471-2105-9-40
pubmed: 18215316
pmcid: 18215316
Roy, A., Kucukural, A. & Zhang, Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725–738, https://doi.org/10.1038/nprot.2010.5 (2010).
doi: 10.1038/nprot.2010.5
pubmed: 20360767
pmcid: 2849174
Yang, J. Y. et al. The I-TASSER Suite: protein structure and function prediction. Nat. Methods. 12, 7–8, https://doi.org/10.1038/nmeth.3213 (2015).
doi: 10.1038/nmeth.3213
pubmed: 25549265
pmcid: 4428668
Ramachandran, S., Kota, P., Ding, F. & Dokholyan, N. V. Automated minimization of steric clashes in protein structures. Proteins. 79, 261–270, https://doi.org/10.1002/prot.22879 (2011).
doi: 10.1002/prot.22879
pubmed: 21058396
pmcid: 3058769
Laskowski, R. A., Moss, D. S. & Thornton, J. M. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231, 1049–1067, https://doi.org/10.1006/jmbi.1993.1351 (1993).
doi: 10.1006/jmbi.1993.1351
pubmed: 8515464
Bowie, J. U., Luthy, R. & Eisenberg, D. A method to identify protein sequences that fold into a known three-dimensional structure. Science. 253, 164–170, https://doi.org/10.1126/science.1853201 (1991).
doi: 10.1126/science.1853201
pubmed: 1853201
Luthy, R., Bowie, J. U. & Eisenberg, D. Assessment of protein models with three-dimensional profiles. Nature. 356, 83–85, https://doi.org/10.1038/356083a0 (1992).
doi: 10.1038/356083a0
pubmed: 1538787
Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795–800, https://doi.org/10.1107/S0021889893005588 (1993).
doi: 10.1107/S0021889893005588
Corpet, F. Multiple sequence alignment with hierarchical clustering. Nucleic. Acids. Res. 16, 10881–10890, https://doi.org/10.1093/nar/16.22.10881 (1988).
doi: 10.1093/nar/16.22.10881
pubmed: 2849754
pmcid: 338945
Gouet, P., Courcelle, E., Stuart, D. I. & Metoz, F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics. 15, 305–308, https://doi.org/10.1093/bioinformatics/15.4.305 (1999).
doi: 10.1093/bioinformatics/15.4.305
pubmed: 10320398
Goswami, S., Das, S. & Datta, S. Understanding the role of residues around the active site tunnel towards generating a glucose-tolerant beta-glucosidase from Agrobacterium tumefaciens 5A. Protein Eng. Des. Sel. 30, 523–530, https://doi.org/10.1093/protein/gzx039 (2017).
doi: 10.1093/protein/gzx039
pubmed: 28873987
Langston, J., Sheehy, N. & Xu, F. Substrate specificity of Aspergillus oryzae family 3 beta-glucosidase. Biochim. Biophys. Acta. 1764, 972–978, https://doi.org/10.1016/j.bbapap.2006.03.009 (2006).
doi: 10.1016/j.bbapap.2006.03.009
pubmed: 16650812
Ximenes, E. A., Felix, C. R. & Ulhoa, C. J. Production of cellulases by Aspergillus fumigatus and characterization of one beta-glucosidase. Curr. Microbiol. 32, 119–123, https://doi.org/10.1007/s002849900021 (1996).
doi: 10.1007/s002849900021
Tiwari, R. et al. Bioprospecting of novel thermostable beta-glucosidase from Bacillus subtilis RA10 and its application in biomass hydrolysis. Biotechnol. Biofuels 10, Artn 24610.1186/S13068-017-0932-8 (2017).
Harada, K. M., Tanaka, K., Fukuda, Y., Hashimoto, W. & Murata, K. Degradation of rice bran hemicellulose by Paenibacillus sp strain HC1: gene cloning, characterization and function of beta-D-glucosidase as an enzyme involved in degradation. Arch. Microbiol. 184, 215–224, https://doi.org/10.1007/s00203-005-0038-8 (2005).
doi: 10.1007/s00203-005-0038-8
pubmed: 16205911
Mamma, D., Hatzinikolaou, D. G. & Christakopoulos, P. Biochemical and catalytic properties of two intracellular beta-glucosidases from the fungus Penicillium decumbens active on flavonoid glucosides. J. Mol. Cata.l B-Enzym. 27, 183–190, https://doi.org/10.1016/j.molcatb.2003.11.011 (2004).
doi: 10.1016/j.molcatb.2003.11.011
Bhat, K. M., Gaikwad, J. S. & Maheshwari, R. Purification and characterization of an extracellular beta-glucosidase from the thermophilic fungus Sporotrichum-thermophile and its influence on cellulase activity. J. Gen. Microbiol. 139, 2825–2832, https://doi.org/10.1099/00221287-139-11-2825 (1993).
doi: 10.1099/00221287-139-11-2825
Korotkova, O. G. et al. Isolation and properties of fungal beta-glucosidases. Biochemistry. Biokhimiia 74, 569–577, https://doi.org/10.1134/s0006297909050137 (2009).
doi: 10.1134/s0006297909050137
pubmed: 19538132