Economical alternatives for the production of fungal β-1,3-glucanase using easily obtainable industrial substrates
DOI:
https://doi.org/10.33448/rsd-v11i14.35856Keywords:
Trichoderma harzianum; Starch; Immobilization; Zymogram; Succinoglycan.Abstract
The β-1,3-glucanases synthesized by filamentous fungi have wide applicability in the food, chemical, and pharmaceutical industries. However, its obtainment can be costly, especially due to substrates used to induce its synthesis. Therefore, the objective of this work was to produce β-1,3-glucanase by T. harzianum Rifai using free and immobilized cells in synthetic and plant sponges, using different inducing substrates that could provide better cost-effectiveness for the industrial production of the enzyme. The Petri dish zymogram technique proved to be efficient for screening substrates inducing β -1,3-glucanases against species of filamentous fungi. It was possible to perform the immobilization of T. harzianum in a synthetic sponge allowing the realization of repetitive batches for enzymatic production. All tested substrates resulted in the synthesis of β-1,3-glucanase, including succinoglycan, proposed innovatively in this study. Fungal biomass resulted in the best inducing substrate under conditions of free and immobilized cells, with a production of β-1,3-glucanases of 0.73 U and 0.80 U of β -1,3-glucanases. The substrates corn starch and cassava showed promise in the production of β-1,3-glucanase and maintained production until the fourth batch was evaluated, with values of 0.51 U and 0.46 U of β-1.3-glucanases, respectively. The results obtained in this study showed that the zymogram is a practical method for screening substrates induced by the fungus T. harzianum. Corn starch and cassava are accessible and low-cost sources for β-1,3-glucanase synthesis in repetitive batches, including the use of immobilized and free cells.
References
Bakhtiyari, M., Moosavi-Nasab, M., & Askari, H. (2015). Optimization of succinoglycan hydrocolloid production by Agrobacterium radiobacter grown in sugar beet molasses and investigation of its physicochemical characteristics. Food Hydrocolloids, 45, 18-29. doi.org/10.1016/j.foodhyd.2014.11.002
Barsanti, L., Vismara, R., Passarelli, V., & Gualtieri, P. (2001). Paramylon (β-1,3-glucan) content in wild type and WZSL mutant of Euglena gracilis. Effects of growth conditions. Journal of applied phycology, 13 (1), 59-65. doi.org/10.1023/A:1008105416065
Bauermeister, A., Amador, I. R., Pretti, C. P., Giese, E. C., & Oliveira, A. L. M. (2015). β-(1→3) Glucanolytic yeasts from Brazilian grape microbiota: production and characterization of β-Glucanolytic enzymes by Aureobasidium pullulans 1WA1 cultivated on fungal mycelium. Journal of agricultural and food chemistry, 63 (1), 269-278. doi.org/10.1021/jf504333h
Bauermeister, A., Rezende, M. I., Giese, E. C., Dekker, R. F. H., & Barbosa, A. M. (2010). β-1,3-Glucanases Fúngicas: produção e aplicações biotecnológicas. Semina: Ciências Exatas e Tecnológicas, 31(2), 75-86. https://www.researchgate.net/
Da Silva, A. L., & Castañeda-Ayarza, J. A. (2021). Macro-environment analysis of the corn ethanol fuel development in Brazil. Renewable and Sustainable Energy Reviews, 135, 110387. doi.org/10.1016/j.rser.2020.110387
De Souza, M. P., Hoeltz, M., Muller, M. V. G., Gressler, P. D., Bjerk, T. R., de Souza Schneider, R. D. C., & Corbellini, V. A. (2019). Screening of fungal strains with potentiality to hydrolyze microalgal biomass by Fourier Transform Infrared Spectroscopy (FTIR). Acta Scientiarum. Technology, 41, e39693-e39693. doi.org/10.4025/actascitechnol.v41i1.39693
Di-Francesco, A., Ugolini, L., Lazzeri, L., & Maria, M. (2015). Production of volatile organic compounds by Aureobasidium pullulans as a potential mechanism of action against postharvest fruit pathogens. Biological Control, 81, 8-14. doi.org/10.1016/j.biocontrol.2014.10.004
EL-Katatny, M. H., Somitsch, W., Robra, K-H., El-Katatny, M. S., & Gübitz, G. M. (2000). Production of chitinase and β-1,3-glucanase by Trichoderma harzianum for control of the phytopathogenic fungus Sclerotium rolfsii. Food Technology and Biotechnology, 38 (3), 173-180. https://www.cabdirect.org/
Gerhardson, B. (2002). Biological substitutes for pesticides. Trends in biotechnology, 20 (8), 338-343. doi.org/10.1016/S0167-7799(02)02021-8
Giese, E. C., Covizzi, L. G., Borsato, D., Dekker, R. F. H., Da Silva, M. D., & Barbosa, A. M. (2005). Botryosphaeran, a new substrate for the production of β-1,3-glucanases by Botryosphaeria rhodina and Trichoderma harzianum Rifai. Process biochemistry, 40 (12), 3783-3788. doi.org/10.1016/j.procbio.2005.04.004
Giese, E. C., Dekker, R. F. H., Scarminio, I. S., Barbosa, A. M., & Da Silva, R. (2011). Comparison of β-1,3-glucanase production by Botryosphaeria rhodina MAMB-05 and Trichoderma harzianum Rifai and its optimization using a statistical mixture-design. Biochemical Engineering Journal, 53 (2), 239-243. doi.org/10.1016/j.bej.2010.10.013
González-Pombo, P. Fariña, L., Carrau, F., & Batista-Viera, F. (2011). A novel extracellular β-glucosidase from Issatchenkia terricola: Isolation, immobilization and application for aroma enhancement of white Muscat wine. Process Biochemistry, 46 (1), 385-389. doi.org/10.1016/j.procbio.2010.07.016
Haapala, R., Linko, S., Parkkinen, E., & Suominen, P. (1994). Production of endo-1,4-β-glucanase and xylanase by Trichoderma reesei immobilized on polyurethane foam. Biotechnology techniques, 8 (6), 401-406. doi.org/10.1007/BF00154311
Hideno, A., Ogbonna, J. C., Aoyagi, H., & Tanaka, H. (2007). Acetylation of loofa (Luffa cylindrica) sponge as immobilization carrier for bioprocesses involving cellulase. Journal of bioscience and bioengineering, 103 (4), 311-317. doi.org/10.1263/jbb.103.311
Howell, C. R. (2003). Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant disease, 87 (1), 4-10. doi.org/10.1094/PDIS.2003.87.1.4
Lopes, M. R., Klein, M. N., Ferraz, L. P., Silva, A. C., & Kupper, K. C. (2015). Saccharomyces cerevisiae: a novel and efficient biological control agent for Colletotrichum acutatum during pre-harvest. Microbiological research, 175, 93-99. doi.org/10.1016/j.micres.2015.04.003
Marcello, C. M., Steindorff, A. S., Silva, S. P., Silva, R. N., Bataus, L., & Ulhoa, C. J. (2010). Expression analysis of the exo-β-1,3-glucanase from the mycoparasitic fungus Trichoderma asperellum. Microbiological Research, 165 (1), 75-81. doi.org/10.1016/j.micres.2008.08.002
Masih, E. I., & Paul, B., (2002). Secretion of β-1,3-glucanases by the yeast Pichia membranifaciens and its possible role in the biocontrol of Botrytis cinerea Causing grey mold disease of the grapevine. Current microbiology, 44 (6), 391-395. doi.org/10.1007/s00284-001-0011-y
Menezes, J. P., Lupatini, M., Antoniolli, Z. I., Blume, E., Junges, E., & Manzoni, C. G. (2010). Variabilidade genética na região its do rDNA de isolados de Trichoderma spp. (Biocontrolador) e Fusarium oxysporum f. sp. chrysanthemi. Ciência e Agrotecnologia, v. 34, 132-139. doi.org/10.1590/S1413-70542010000100017
Musoni, M., Destain, J., Thonart, P., Bahama, J-B., & Delvigne F. (2015). Bioreactor design and implementation strategies for the cultivation of filamentous fungi and the production of fungal metabolites: from traditional methods to engineered systems. Biotechnol. Agron. Soc. Environ, 19 (4), 430-442. https://popups.uliege.be/
Nelson, N. (1994). A photometric adaptation of the Somogyi method for the determination of glucose. Journal of biological chemistry, 153 (2), 375-380. http://www.jbc.org/
Pazzetto, R., Delina, T. C. O., Fenelon, V. C., & Matioli, G. (2011). Cyclodextrin production by Bacillus firmus strain 37 cells immobilized on loofa sponge. Process biochemistry, 46 (1), 46-51. doi.org/10.1016/j.procbio.2010.07.008
Pitson, S. M., Seviour, R. J., & Mcdougall, B. M. (1993). Noncellulolytic fungal β-glucanases: their physiology and regulation. Enzyme and microbial technology, 15 (3), 178-192. doi.org/10.1016/0141-0229(93)90136-P
Ramada, M. H. S., Steindorff, A. S., Jr Bloch, C., & Ulhoa, C. J. (2016). Secretome analysis of the mycoparasitic fungus Trichoderma harzianum ALL 42 cultivated in different media supplemented with Fusarium solani cell wall or glucose. Proteomics, 16 (3), 477-490. doi.org/10.1002/pmic.201400546
Rao, K. L. N., Raju, K. S., & Ravisankar, H. (2016). Cultural conditions on the production of extracellular enzymes by Trichoderma isolates from tobacco rhizosphere. Brazilian journal of microbiology, 47, 25-32. doi.org/10.1016/j.bjm.2015.11.007
Rezende, M. I., Barbosa, A. M., Vasconcelos, A. F. D., & Endo, A. S. (2002). Xylanase production by Trichoderma harzianum Rifai by solid state fermentation on sugarcane bagasse. Brazilian Journal of Microbiology, 33, 67-72. doi.org/10.1590/S1517-83822002000100014
Ruiz, S. P., Martinez, C. O., Noce, A. S., Sampaio, A. R., Baesso, M. L., & Matioli, G. (2015). Biosynthesis of succinoglycan by Agrobacterium radiobacter NBRC 12665 immobilized on loofa sponge and cultivated in sugar cane molasses. Structural and rheological characterization of biopolymer. Journal of Molecular Catalysis B: Enzymatic, 122, 15-28. doi.org/10.1016/j.molcatb.2015.08.016
Santos, V. A. Q., & Cruz, C. H. G. (2016). Ethanol and Levan production by sequential bath using Zymomonas mobilis immobilized on alginate and chitosan beads. Acta Scientiarum. Technology, 38(3), 263-271. doi.org/10.4025/actascitechnol.v38i3.27646
Sharma, K., Mishra, A. K., & Misra, R. S. (2009). Morphological, biochemical and molecular characterization of Trichoderma harzianum isolates for their efficacy as biocontrol agents. Journal of Phytopathology, 157 (1), 51-56. doi.org/10.1111/j.1439-0434.2008.01451.x
Stubbs, H. J., Brasch, D. J., Emerson, G. W., & Sullivan, P. A. (1999). Hydrolase and transferase activities of the β‐1,3‐exoglucanase of Candida albicans. European journal of biochemistry, 263 (3), 889-895. doi.org/10.1046/j.1432-1327.1999.00581.x
Syed, S., Riyaz-Ul-Hassan, S., & Johri, S. (2013). A novel cellulase from an endophyte, Penicillium sp. NFCCI 2862. American Journal of Microbiological Research, 1 (4), 84-91. doi.org/ 10.12691/ajmr-1-4-4
Usoltseva, R. V., Belik, A. A., Kusaykin, M., Malyarenko, O. S., Zvyagintseva, T. N., & Ermakova, S., (2020). Laminarans and 1, 3-β-D-glucanases. International Journal of Biological Macromolecules, 163, 1010-1025. doi.org/10.1016/j.ijbiomac.2020.07.034
Vázquez-Garcidueñas, S., Leal-Morales, C. A., & Herrera-Estrella, A. (1998). Analysis of the β-1,3-glucanolytic system of the biocontrol agent Trichoderma harzianum. Applied and environmental microbiology, 64 (4), 1442-1446. doi.org/10.1128/AEM.64.4.1442-1446.1998
Vero, S., Garmendia, G., González, M. B., Garat M. F., & Wisniewski, M. (2009). Aureobasidium pullulans as a biocontrol agent of postharvest pathogens of apples in Uruguay. Biocontrol Science and Technology, 19 (10), 1033-1049. doi.org/10.1080/09583150903277738
Vilpoux, O. (2011). Desempenho dos arranjos institucionais e minimização dos custos de transação: transações entre produtores e fecularias de mandioca. Revista de Economia e Sociologia Rural, 49, 271-294. doi.org/10.1590/S0103-20032011000200001
Vogel, H. J. (1956). A convenient growth medium for Neurospora crassa. Microbial genetics bulletin. 13, 42-43.
Yu, B., Zhang, X., Sun, W., Xi, X., Zhao, N., Huang, Z., Ying, Z., Liu, L., Liu, D., Niu, H., Wu, J., Zhuang, W., Zhu, C., Chen, Y., & Ying, H. (2018). Continuous citric acid production in repeated-fed batch fermentation by Aspergillus niger immobilized on a new porous foam. Journal of biotechnology, 276, 1-9. doi.org/10.1016/j.jbiotec.2018.03.015
Zhang, D., Spadaro, D., Garibaldi, A., & Gullino, M. L. (2010). Efficacy of the antagonist Aureobasidium pullulans PL5 against postharvest pathogens of peach, apple and plum and its modes of action. Biological Control, 54 (3), 172-180. doi.org/10.1016/j.biocontrol.2010.05.003
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