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Research Articles

Two β-glucanases from bacterium Cellulomonas flavigena: expression in Pichia pastoris, properties, biotechnological potential

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References

  • Synytsya, A.; Novak, M. Structural Analysis of Glucans. Ann. Transl. Med. 2014, 2, 17–31. DOI: 10.3978/j.issn.2305-5839.2014.02.07.
  • Schmid, J.; Meyer, V.; Sieber, V. Scleroglucan: Biosynthesis, Production and Application of a Versatile Hydrocolloid. Appl. Microbiol. Biotechnol. 2011, 91, 937–947. DOI: 10.1007/s00253-011-3438-5.
  • Du, B.; Meenu, M.; Liu, H.; Xu, B. A Concise Review on the Molecular Structure and Function Relationship of β-Glucan. Int. J. Mol. Sci. 2019, 20, 4032–4050. DOI: 10.3390/ijms20164032.
  • Agger, J. W.; Isaksen, T.; Várnai, A.; Vidal-Melgosa, S.; Willats, W. G.; Ludwig, R.; Horn, S. J.; Eijsink, V. G.; Westereng, B. Discovery of LPMO Activity on Hemicelluloses Shows the Importance of Oxidative Processes in Plant Cell Wall Degradation. Proc. Natl. Acad. Sci. U.S.A. 2014, 111, 6287–6292. DOI: 10.1073/pnas.1323629111.
  • Liu, Y.; Dun, B.; Shi, P.; Ma, R.; Luo, H.; Bai, Y.; Xie, X.; Yao, B. A Novel GH7 Endo-β-1,4-Glucanase from Neosartorya fischeri P1 with Good Thermostability, Broad Substrate Specificity and Potential Application in the Brewing Industry. PLOS One 2015, 10, e0137485. DOI: 10.1371/journal.pone.0137485.
  • Li, C.; Wen, Y.; He, Y.; Zhu, J.; Yin, X.; Yang, J.; Zhang, L.; Song, L.; Xia, X.; Yu, R. Purification and Characterization of a Novel β-1,3-Glucanase from Arca inflata and Its Immune-Enhancing Effects. Food Chem. 2019, 290, 1–9. DOI: 10.1016/j.foodchem.2019.03.131.
  • Hrmova, M.; Harvey, A. J.; Wang, J.; Shirley, N. J.; Jones, G. P.; Stone, B. A.; Høj, P. B.; Fincher, G. B. Barley β-D-Glucan Exohydrolases with β-D-Glucosidase Activity. Purification, Characterization, and Determination of Primary Structure from a cDNA Clone. J. Biol. Chem. 1996, 271, 5277–5286. DOI: 10.1074/jbc.271.9.5277.
  • Vijayendra, S. V.; Kashiwagi, Y. Characterization of a New Acid Stable Exo-β-1,3-Glucanase of Rhizoctonia solani and Its Action on Microbial Polysaccharides. Int. J. Biol. Macromol. 2009, 44, 92–97. DOI: 10.1016/j.ijbiomac.2008.10.008.
  • Wang, J.; Kang, L.; Liu, Z.; Yuan, S. Gene Cloning, Heterologous Expression and Characterization of a Coprinopsis cinerea Endo-β-1,3(4)-Glucanase. Fungal Biol. 2017, 121, 61–68. DOI: 10.1016/j.funbio.2016.09.003.
  • Planas, A. Bacterial 1,3-1,4-β-Glucanases: Structure, Function and Protein Engineering. Biochim. Biophys. Acta 2000, 1543, 361–382. DOI: 10.1016/s0167-4838(00)00231-4.
  • Müller, J. J.; Thomsen, K. K.; Heinemann, U. Crystal Structure of Barley 1,3-1,4-β-Glucanase at 2.0-A Resolution and Comparison with Bacillus 1,3-1,4-β-Glucanase. J. Biol. Chem. 1998, 273, 3438–3446. DOI: 10.1074/jbc.273.6.3438.
  • Kumagai, Y.; Ojima, T. Isolation and Characterization of Two Types of β-1,3-Glucanases from the Common Sea Hare Aplysia kurodai. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2010, 155, 138–144. DOI: 10.1016/j.cbpb.2009.10.013.
  • Sharma, A.; Nakas, J. P. Preliminary Characterization of Laminarinase from Trichoderma longibrachiatum. Enzyme Microb. Technol. 1987, 9, 89–93. DOI: 10.1016/0141-0229(87)90148-7.
  • Bamforth, C. W.; Martin, H. L. The Degradation of β-Glucan during Malting and Mashing – The Role of β-Glucanase. J. Inst. Brewing 1983, 89, 303–307. DOI: 10.1002/j.2050-0416.1983.tb04190.x.
  • Chaari, F.; Belghith-Fendri, L.; Blibech, M.; Driss, D.; Ellouzi, S.; Sameh, M.; Ellouz-Chaabouni, S. Biochemical Characterization of a Lichenase from Penicillium occitanis Pol6 and Its Potential Application in the Brewing Industry. Process Biochem. 2014, 49, 1040–1046. DOI: 10.1016/j.procbio.2014.02.023.
  • Almirall, M.; Francesch, M.; Perez-Vendrell, A. M.; Brufau, J.; Esteve-Garcia, E. The Differences in Intestinal Viscosity Produced by Barley and β-Glucanase Alter Digesta Enzyme Activities and Ileal Nutrient Digestibilities More in Broiler Chicks than in Cocks. J. Nutr. 1995, 125, 947–955.
  • Fernandes, V. O.; Costa, M.; Ribeiro, T.; Serrano, L.; Cardoso, V.; Santos, H.; Lordelo, M.; Ferreira, L. M. A.; Fontes, C. 1,3-1,4-β-Glucanases and Not 1,4-β-Glucanases Improve the Nutritive Value of Barley-Based Diets for Broilers. Animal Feed Sci. Technol. 2016, 211, 153–163. DOI: 10.1016/j.anifeedsci.2015.11.007.
  • Mitmesser, S.; Combs, M. Prebiotics: Inulin and Other Oligosaccharides. In The Microbiota in Gastrointestinal Pathophysiology; Floch, M. H., Ringel, Y., Walker, W. A., Eds.; Academic Press: Massachusetts; 2017, pp 201–208.
  • Fehlbaum, S.; Prudence, K.; Kieboom, J.; Heerikhuisen, M.; van den Broek, T.; Schuren, F. H. J.; Steinert, R. E.; Raederstorff, D. In Vitro Fermentation of Selected Prebiotics and Their Effects on the Composition and Activity of the Adult Gut Microbiota. Int. J. Mol. Sci. 2018, 19, 3097–3313. DOI: 10.3390/ijms19103097.
  • Sims, I. M.; Ryan, J. L.; Kim, S. H. In Vitro Fermentation of Prebiotic Oligosaccharides by Bifidobacterium lactis HN019 and Lactobacillus spp. Anaerobe 2014, 25, 11–17. DOI: 10.1016/j.anaerobe.2013.11.001.
  • Christopherson, M. R.; Suen, G.; Bramhacharya, S.; Jewell, K. A.; Aylward, F. O.; Mead, D.; Brumm, P. J. The Genome Sequences of Cellulomonas fimi and “Cellvibrio gilvus” Reveal the Cellulolytic Strategies of Two Facultative Anaerobes, Transfer of “Cellvibrio gilvus” to the Genus Cellulomonas, and Proposal of Cellulomonas gilvus sp. PLOS One 2013, 8, e53954. DOI: 10.1371/journal.pone.0053954.
  • Mayorga-Reyes, L.; Morales, Y.; Salgado, L. M.; Ortega, A.; Ponce-Noyola, T. Cellulomonas flavigena: Characterization of an Endo-1,4-Xylanase Tightly Induced by Sugarcane Bagasse. FEMS Microbiol. Lett. 2002, 214, 205–209. DOI: 10.1111/j.1574-6968.2002.tb11348.x.
  • Kamennaya, N. A.; Gray, J.; Ito, S.; Kainuma, M.; Nguyen, M. V.; Khilyas, I. V.; Birarda, G.; Bernie, F.; Hunt, M.; Vasadia, D.; et al. Deconstruction of Plant Biomass by a Cellulomonas Strain Isolated from an Ultra-Basic (Lignin-Stripping) Spring. Arch. Microbiol. 2020, 202, 1077–1084. DOI: 10.1007/s00203-020-01816-z.
  • Lisov, A. V.; Belova, O. V.; Lisova, Z. A.; Vinokurova, N. G.; Nagel, A. S.; Andreeva-Kovalevskaya, Z. I.; Budarina, Z. I.; Nagornykh, M. O.; Zakharova, M. V.; Shadrin, A. M.; et al. Xylanases of Cellulomonas flavigena: Expression, Biochemical Characterization, and Biotechnological Potential. AMB Express 2017, 7, 5. DOI: 10.1186/s13568-016-0308-7.
  • Ríos-Fránquez, F. J.; González-Bautista, E.; Ponce-Noyola, T.; Ramos-Valdivia, A. C.; Poggi-Varaldo, H. M.; García-Mena, J.; Martinez, A. Expression of a Codon-Optimized β-Glucosidase from Cellulomonas flavigena PR-22 in Saccharomyces cerevisiae for Bioethanol Production from Cellobiose. Arch. Microbiol. 2017, 199, 605–611. DOI: 10.1007/s00203-016-1333-2.
  • Saxena, H.; Hsu, B.; de Asis, M.; Zierke, M.; Sim, L.; Withers, S. G.; Wakarchuk, W. Characterization of a Thermostable Endoglucanase from Cellulomonas fimi ATCC484. Biochem. Cell Biol. 2018, 96, 68–76. DOI: 10.1139/bcb-2017-0150.
  • Rojas-Rejón, Ó. A.; Poggi-Varaldo, H. M.; Ramos-Valdivia, A. C.; Ponce-Noyola, T.; Cristiani-Urbina, E.; Martínez, A.; de la Torre, M. Enzymatic Saccharification of Sugar Cane Bagasse by Continuous Xylanase and Cellulase Production from Cellulomonas flavigena PR-22. Biotechnol. Prog. 2016, 32, 321–326. DOI: 10.1002/btpr.2213.
  • Wood, T. M. Preparation of Crystalline, Amorphous and Dyed Cellulose Substrates. Methods Enzymol. 1988, 160, 19–25.
  • Ghose, T. K. Measurement of Cellulase Activities. Pure Appl. Chem. 1987, 59, 257–268. DOI: 10.1351/pac198759020257.
  • Lisov, A. V.; Belova, O. V.; Andreeva-Kovalevskaya, Z. I.; Budarina, Z. I.; Solonin, A. A.; Vinokurova, N. G.; Leontievsky, A. A. Recombinant Xylanase from Streptomyces coelicolor Ac-738: Characterization and the Effect on Xylan-Containing Products. World J. Microbiol. Biotechnol. 2014, 30, 801–808. DOI: 10.1007/s11274-013-1480-4.
  • Cereghino, J. L.; Cregg, J. M. Heterologous Protein Expression in the Methylotrophic Yeast Pichia pastoris. FEMS Microbiol. Rev. 2000, 24, 45–66. DOI: 10.1111/j.1574-6976.2000.tb00532.x.
  • Looser, V.; Bruhlmann, B.; Bumbak, F.; Stenger, C.; Costa, M.; Camattari, A.; Fotiadis, D.; Kovar, K. Cultivation Strategies to Enhance Productivity of Pichia pastoris: A Review. Biotechnol. Adv. 2015, 33, 1177–1193. DOI: 10.1016/j.biotechadv.2015.05.008.
  • Zhang, P.; Zhang, W.; Zhou, X.; Bai, P.; Cregg, J. M.; Zhang, Y. Catabolite Repression of AOX in Pichia pastoris is Dependent on Hexose Transporter PpHxt1 and Pexophagy. Appl. Environ. Microbiol. 2010, 76, 6108–6118. DOI: 10.1128/AEM.00607-10.
  • Lau, A. T.; Wong, W. K. Purification and Characterization of a Major Secretory Cellobiase, Cba2, from Cellulomonas biazotea. Protein Expr. Purif. 2001, 23, 159–166. DOI: 10.1006/prep.2001.1486.
  • Rapp, P.; Wagner, F. Production and Properties of Xylan-Degrading Enzymes from Cellulomonas uda. Appl. Environ. Microbiol. 1986, 51, 746–752. DOI: 10.1128/aem.51.4.746-752.1986.
  • Hitchner, E. V.; Leatherwood, J. M. Use of a Cellulase-Derepressed Mutant of Cellulomonas in the Production of a Single-Cell Protein Product from Cellulose. Appl. Environ. Microbiol. 1980, 39, 382–386. DOI: 10.1128/aem.39.2.382-386.1980.
  • Barrera-Islas, G. A.; Ramos-Valdivia, A. C.; Salgado, L. M.; Ponce-Noyola, T. Characterization of a β-Glucosidase Produced by a High-Specific Growth-Rate Mutant of Cellulomonas flavigena. Curr. Microbiol. 2007, 54, 266–270. DOI: 10.1007/s00284-006-0105-7.
  • Rajoka, M. I.; Durrani, I. S.; Khalid, A. M. Kinetics of Improved Production and Thermostability of an Intracellular β a-Glucosidase from a Mutant-Derivative of Cellulomonas biazotea. Biotechnol. Lett. 2004, 26, 281–285. DOI: 10.1023/b:bile.0000015426.74418.07.
  • Gao, J.; Wakarchuk, W. Characterization of Five β-Glycoside Hydrolases from Cellulomonas fimi ATCC 484. J. Bacteriol. 2014, 196, 4103–4110. DOI: 10.1128/JB.02194-14.
  • Pérez-Avalos, O.; Sánchez-Herrera, L. M.; Salgado, L. M.; Ponce-Noyola, T. A Bifunctional Endoglucanase/Endoxylanase from Cellulomonas flavigena with Potential Use in Industrial Processes at Different pH. Curr. Microbiol. 2008, 57, 39–44. DOI: 10.1007/s00284-008-9149-1.
  • Gutiérrez-Nava, A.; Herrera-Herrera, A.; Mayorga-Reyes, L.; Salgado, L. M.; Ponce-Noyola, T. Expression and Characterization of the celcflB Gene from Cellulomonas flavigena Encoding an Endo-β-1,4-Glucanase. Curr. Microbiol. 2003, 47, 359–363. DOI: 10.1007/s00284-002-4016-y.
  • Ferrer, P.; Halkier, T.; Hedegaard, L.; Savva, D.; Diers, I.; Asenjo, J. A. Nucleotide Sequence of a β-1,3-Glucanase Isoenzyme IIA Gene of Oerskovia xanthineolytica LL G109 (Cellulomonas cellulans) and Initial Characterization of the Recombinant Enzyme Expressed in Bacillus subtilis. J. Bacteriol. 1996, 178, 4751–4757. DOI: 10.1128/jb.178.15.4751-4757.1996.
  • Paradis, F. W.; Warren, R. A.; Kilburn, D. G.; Miller, R. C. Jr. The Expression of Cellulomonas fimi Cellulase Genes in Brevibacterium lactofermentum. Gene 1987, 61, 199–206. DOI: 10.1016/0378-1119(87)90114-4.
  • Curry, C.; Gilkes, N.; O'neill, G.; Miller, R. C.; Skipper, N. Expression and Secretion of a Cellulomonas fimi Exoglucanase in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 1988, 54, 476–484. DOI: 10.1128/aem.54.2.476-484.1988.
  • Kim, C. K.; Choi, H. S.; Lee, S. J.; Lee, J. H.; Lee, J. H.; Yoo, H. Y.; Han, S. O.; Kim, S. W. Production of Xylanase from a Novel Engineered Pichia pastoris and Application to Enzymatic Hydrolysis Process for Biorefinery. Process Biochem. 2018, 65, 130–135. DOI: 10.1016/j.procbio.2017.11.001.
  • Cayetano-Cruz, M.; Pérez de los Santos, A. I.; García-Huante, Y.; Santiago-Hernández, A.; Pavón-Orozco, P.; López y López, V. E.; Hidalgo-Lara, M. E. High Level Expression of a Recombinant Xylanase by Pichia pastoris Cultured in a Bioreactor with Methanol as the Sole Carbon Source: Purification and Biochemical Characterization of the Enzyme. Biochem. Engineer. J. 2016, 112, 161–169. DOI: 10.1016/j.bej.2016.04.014.
  • Liu, X.; Jiang, Z.; Ma, S.; Yan, Q.; Chen, Z.; Liu, H. High-Level Production and Characterization of a Novel β-1,3-1,4-Glucanase from Aspergillus awamori and Its Potential Application in the Brewing Industry. Process Biochem. 2020, 92, 252–260. DOI: 10.1016/j.procbio.2020.01.017.
  • Hua, C.; Yan, Q.; Jiang, Z.; Li, Y.; Katrolia, P. High-Level Expression of a Specific Beta-1,3-1,4-Glucanase from the Thermophilic Fungus Paecilomyces thermophila in Pichia pastoris. Appl. Microbiol. Biotechnol. 2010, 88, 509–518. DOI: 10.1007/s00253-010-2759-0.
  • Huang, H.; Yang, P.; Luo, H.; Tang, H.; Shao, N.; Yuan, T.; Wang, Y.; Bai, Y.; Yao, B. High-Level Expression of a Truncated 1,3-1,4-β-D-Glucanase from Fibrobacter succinogenes in Pichia pastoris by Optimization of Codons and Fermentation. Appl. Microbiol. Biotechnol. 2008, 78, 95–103. DOI: 10.1007/s00253-007-1290-4.
  • Spohner, S. C.; Müller, H.; Quitmann, H.; Czermak, P. Expression of Enzymes for the Usage in Food and Feed Industry with Pichia pastoris. J. Biotechnol. 2015, 202, 118–134. DOI: 10.1016/j.jbiotec.2015.01.027.
  • Chen, H.; Li, X. L.; Ljungdahl, L. G. Sequencing of a 1,3-1,4-beta-D-Glucanase (Lichenase) from the Anaerobic Fungus Orpinomyces Strain PC-2: properties of the Enzyme Expressed in Escherichia coli and Evidence That the Gene Has a Bacterial Origin. J. Bacteriol. 1997, 179, 6028–6034. DOI: 10.1128/jb.179.19.6028-6034.1997.
  • Bretthauer, R. K.; Castellino, F. J. Glycosylation of Pichia pastoris-Derived Proteins. Biotechnol. Appl. Biochem. 1999, 30, 193–200.
  • Boraston, A. B.; Warren, R. A.; Kilburn, D. G. Glycosylation by Pichia pastoris Decreases the Affinity of a Family 2a Carbohydrate-Binding Module from Cellulomonas fimi: A Functional and Mutational Analysis. Biochem. J. 2001, 358, 423–430. DOI: 10.1042/0264-6021:3580423.
  • Grishutin, S. G.; Gusakov, A. V.; Dzedzyulya, E. I.; Sinitsyn, A. P. A Lichenase-like Family 12 Endo-(1-4)-β-Glucanase from Aspergillus japonicus: Study of the Substrate Specificity and Mode of Action on β-Glucans in Comparison with Other Glycoside Hydrolases. Carbohydr. Res. 2006, 341, 218–229. DOI: 10.1016/j.carres.2005.11.011.
  • Chen, Y.-C.; Chen, W.-T.; Liu, J.-C.; Tsai, L.-C.; Cheng, H.-L. A Highly Active Beta-Glucanase from a New Strain of Rumen Fungus Orpinomyces sp. Y102 Exhibits Cellobiohydrolase and Cellotriohydrolase Activities. Bioresour. Technol. 2014, 170, 513–521. DOI: 10.1016/j.biortech.2014.08.016.
  • Wong, W. K.; Gerhard, B.; Guo, Z. M.; Kilburn, D. G.; Warren, A. J.; Miller, R. C. Jr. Characterization and Structure of an Endoglucanase Gene cenA of Cellulomonas fimi. Gene 1986, 44, 315–324. DOI: 10.1016/0378-1119(86)90196-4.
  • Gilkes, N. R.; Warren, R. A.; Miller, R. C.; Jr.; Kilburn, D. G. Precise Excision of the Cellulose Binding Domains from Two Cellulomonas fimi Cellulases by a Homologous Protease and the Effect on Catalysis. J. Biol. Chem. 1988, 263, 10401–10407.
  • Meinke, A.; Gilkes, N. R.; Kwan, E.; Kilburn, D. G.; Warren, R. A.; Miller, R. C. Jr. Cellobiohydrolase A (CbhA) from the Cellulolytic Bacterium Cellulomonas fimi is a Beta-1,4-Exocellobiohydrolase Analogous to Trichoderma reesei CBH II. Mol. Microbiol. 1994, 12, 413–422. DOI: 10.1111/j.1365-2958.1994.tb01030.x.
  • Li, F.; Dong, J.; Lv, X.; Wen, Y.; Chen, S. Recombinant Expression and Characterization of Two Glycoside Hydrolases from Extreme Alklinphilic Bacterium Cellulomonas bogoriensis 69B4T. AMB Express 2020, 10, 44. DOI: 10.1186/s13568-020-00979-8.
  • Erfle, J. D.; Teather, R. M.; Wood, P. J.; Irvin, J. E. Purification and Properties of a β-1,3-1,4-Glucanase (Lichenase, 1,3-1,4-β-D-Glucan 4-Glucanohydrolase, EC 3.2.1.73) from Bacteroides succinogenes Cloned in Escherichia coli. Biochem. J. 1988, 255, 833–841. DOI: 10.1042/bj2550833.
  • Yoo, D. H.; Lee, B. H.; Chang, P. S.; Lee, H. G.; Yoo, S. H. Improved Quantitative Analysis of Oligosaccharides from Lichenase Hydrolyzed Water-Soluble Barley β-Glucans by Highperformance Anion-Exchange Chromatography. J. Agric. Food Chem. 2007, 55, 1656–1662. DOI: 10.1021/jf062603l.
  • Mikkelsen, M. S.; Jespersen, B. M.; Larsen, F. H.; Blennow, A.; Engelsen, S. B. Molecular Structure of Large-Scale Extracted β-Glucan from Barley and Oats: Identification of a Significantly Changed Block Structure in a High β-Glucan Barley Mutant. Food Chem. 2013, 136, 130–138. DOI: 10.1016/j.foodchem.2012.07.097.
  • Rodehutscord, M.; Rückert, C.; Maurer, H. P.; Schenkel, H.; Schipprack, W.; Bach  , Knudsen, K. E.; Schollenberger, M.; Laux, M.; Eklund, M.; Siegert, W.; et al. Variation in Chemical Composition and Physical Characteristics of Cereal Grains from Different Genotypes. Arch. Anim. Nutr. 2016, 70, 87–107. DOI: 10.1080/1745039X.2015.1133111.
  • Cho, K. C.; White, P. J. Enzymatic Analysis of β-Glucan Content in Different Oat Genotypes. Cereal Chem. 1993, 70, 539–542.

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