Abstract
Cell wall degrading enzymes (chitinase and β-1,3-glucanase) were produced by solid-state fermentation (SSF) using the fungus Trichoderma harzianum and different agro-industrial products, mainly residues. The influence of temperature (25–35 °C), initial moisture content (50–90% w/w), nutrient solution (1–2% v/w), and yeast extract (1–2% w/w) on enzyme activity was evaluated. The application of ultrasound during fermentation for different times (0–6 h/day) was also studied. White rice was the substrate that showed the highest chitinase and β-1,3-glucanase activities, which were 31.31 U/g for chitinase and 23.83 U/g for β-1,3-glucanase after 10 days of fermentation. Application of ultrasound waves during fermentation positively affected (p < 0.05) the enzyme activities. The best results for chitinase (51.88 U/g) and β-1,3-glucanase (39.22 U/g) were obtained with a 50% (w/w) moisture content and 4 h/day ultrasound application for 10 days of fermentation. Increases of 3.6-fold (from 14.37 to 51.88 U/g) and 3.8-fold (from 10.22 to 39.22 U/g) in activities for chitinase and β-1,3-glucanase, respectively, compared to non-sonicated fermentation, were obtained. Ultrasound technique associated with the SSF process was a promising alternative to increase the production activity of cell wall degrading enzymes: chitinase and β-1,3-glucanase.
Similar content being viewed by others
References
Aita BC, Spannemberg SS, Schmaltz S et al (2019) Production of cell-wall degrading enzymes by solid-state fermentation using agroindustrial residues as substrates. J Environ Chem Eng 7:103193. https://doi.org/10.1016/j.jece.2019.103193
Aita BC, Schmaltz S, Fochi A et al (2022) Spray-dried powder containing chitinase and β-1,3-glucanase with insecticidal activity against Ceratitis capitata (Diptera: Tephritidae). Processes 10:587. https://doi.org/10.3390/pr10030587
Alves EA, Schmaltz S, Tres MV et al (2020) Process development to obtain a cocktail containing cell-wall degrading enzymes with insecticidal activity from Beauveria bassiana. Biochem Eng J. https://doi.org/10.1016/j.bej.2019.107484
Avhad DN, Rathod VK (2014) Ultrasound stimulated production of a fibrinolytic enzyme. Ultrason Sonochem 21:182–188. https://doi.org/10.1016/j.ultsonch.2013.05.013
Avhad DN, Rathod VK (2015) Ultrasound assisted production of a fibrinolytic enzyme in a bioreactor. Ultrason Sonochem 22:257–264. https://doi.org/10.1016/j.ultsonch.2014.04.020
Bai Z, Jin B, Li Y et al (2008) Utilization of winery wastes for Trichoderma viride biocontrol agent production by solid state fermentation. J Environ Sci 20:353–358. https://doi.org/10.1016/S1001-0742(08)60055-8
Baldoni DB, Antoniolli ZI, Mazutti MA et al (2020) Chitinase production by Trichoderma koningiopsis UFSMQ40 using solid state fermentation. Braz J Microbiol 51:1897–1908. https://doi.org/10.1007/s42770-020-00334-w
Baron NC, Rigobelo EC, Zied DC (2019) Filamentous fungi in biological control: current status and future perspectives. Chil J Agric Res 79:307–315. https://doi.org/10.4067/S0718-58392019000200307
Bhanu Prakash GVS, Padmaja V, Siva Kiran RR (2008) Statistical optimization of process variables for the large-scale production of Metarhizium anisopliae conidiospores in solid-state fermentation. Bioresour Technol 99:1530–1537. https://doi.org/10.1016/j.biortech.2007.04.031
Binod P, Sandhya C, Suma P et al (2007) Fungal biosynthesis of endochitinase and chitobiase in solid state fermentation and their application for the production of N-acetyl-d-glucosamine from colloidal chitin. Bioresour Technol 98:2742–2748. https://doi.org/10.1016/j.biortech.2006.09.030
Blauth de Lima F, Félix C, Osório N et al (2017) Trichoderma harzianum T1A constitutively secretes proteins involved in the biological control of Guignardia citricarpa. Biol Control 106:99–109. https://doi.org/10.1016/j.biocontrol.2017.01.003
Boukaew S, Petlamul W, Suyotha W, Prasertsan P (2016) Simultaneous fermentative chitinase and β-1,3 glucanase production from Streptomyces philanthi RM-1-1-38 and their antifungal activity against rice sheath blight disease. Biotechnologia 97:271–284. https://doi.org/10.5114/bta.2016.64544
Brun T, Rabuske J, Confortin TC et al (2022) Weed control by metabolites produced from Diaporthe schini. Environ Technol 43:139–148. https://doi.org/10.1080/09593330.2020.1780477
de Carvalho Silvello MA, Martínez J, Goldbeck R (2020) Low-frequency ultrasound with short application time improves cellulase activity and reducing sugars release. Appl Biochem Biotechnol 191:1042–1055. https://doi.org/10.1007/s12010-019-03148-1
De La Cruz QR, Roussos S, Hernández D et al (2015) Challenges and opportunities of the bio-pesticides production by solid-state fermentation: filamentous fungi as a model. Crit Rev Biotechnol 35:326–333. https://doi.org/10.3109/07388551.2013.857292
Dos Reis CBL, Sobucki L, Mazutti MA et al (2018) Production of chitinase from Metarhizium anisopliae by solid-state fermentation using sugarcane bagasse as substrate. Ind Biotechnol 14:230–234. https://doi.org/10.1089/ind.2017.0031
Ekundayo EA, Ekundayo FO, Bamidele F (2016) Production, partial purification and optimization of a chitinase produced from Trichoderma viride, an isolate of maize cob. Mycosphere 7:786–793. https://doi.org/10.5943/mycosphere/7/6/9
El-Katatny MH, Gudelj M, Robra KH et al (2001) Characterization of a chitinase and an endo-β-1,3-glucanase from Trichoderma harzianum Rifai T24 involved in control of the phytopathogen Sclerotium rolfsii. Appl Microbiol Biotechnol 56:137–143. https://doi.org/10.1007/s002530100646
Farag MA, Al-Nusarie ST, Farag MA et al (2014) Production, optimization, characterization and antifungal activity of chitinase produced by Aspergillus terrus. Afr J Biotechnol 13:1567–1578. https://doi.org/10.5897/ajb2014.13628
Galván-D’Alessandro L, Carciochi RA (2018) Fermentation assisted by pulsed electric field and ultrasound: a review. Fermentation 4:1–12. https://doi.org/10.3390/fermentation4010001
García-Fraga B, da Silva AF, López-Seijas J, Sieiro C (2015) Optimized expression conditions for enhancing production of two recombinant chitinolytic enzymes from different prokaryote domains. Bioprocess Biosyst Eng 38:2477–2486. https://doi.org/10.1007/s00449-015-1485-5
Giese E, Dekker R, Barbosa A et al (2011) Production of β-(1,3)-glucanases by Trichoderma harzianum Rifai: Optimization and Application to Produce Gluco-oligosaccharides from Paramylon and Pustulan. Ferment Technol 1:1–5. https://doi.org/10.4172/2167-7972
Harman GE, Howell CR, Viterbo A et al (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56. https://doi.org/10.1038/nrmicro797
Islam MN, Zhang M, Adhikari B (2014) The inactivation of enzymes by ultrasound-a review of potential mechanisms. Food Rev Int 30:1–21. https://doi.org/10.1080/87559129.2013.853772
Jaronski ST (2014) Mass production of entomopathogenic fungi: State of the art. In: Mass production of beneficial organisms: invertebrates and entomopathogens. Academic Press, pp 357–413
Jaronski S, Jackson M (2012) Mass Production of entomopathogenic Hypocreales. In: Lacey L (ed) Manual of techniques in invertebrate pathology, Second. Academic Press, New York, pp 255–284
Jiang C, Song J, Cong H et al (2017) Expression and characterization of a novel antifungal exo-β-1,3-glucanase from Chaetomium cupreum. Appl Biochem Biotechnol 182:261–275. https://doi.org/10.1007/s12010-016-2325-z
Karthik N, Akanksha K, Binod P, Pandey A (2014) Production, purification and properties of fungal chitinases—a review. Indian J Exp Biol 52:1025–1035
Kumar DP, Singh RK, Anupama PD et al (2012) Studies on Exo-chitinase production from Trichoderma asperellum UTP-16 and its characterization. Indian J Microbiol 52:388–395. https://doi.org/10.1007/s12088-011-0237-8
Kwiatkowska B, Bennett J, Akunna J et al (2011) Stimulation of bioprocesses by ultrasound. Biotechnol Adv 29:768–780. https://doi.org/10.1016/j.biotechadv.2011.06.005
Leaes EX, Lima D, Miklasevicius L et al (2013) Effect of ultrasound-assisted irradiation on the activities of α-amylase and amyloglucosidase. Biocatal Agric Biotechnol 2:21–25. https://doi.org/10.1016/j.bcab.2012.08.003
Luft L, Confortin TC, Todero I et al (2021) Extraction and characterization of polysaccharide-enriched fractions from Phoma dimorpha mycelial biomass. Bioprocess Biosyst Eng 2:21–25. https://doi.org/10.1007/s00449-020-02486-3
Ma X, Wang W, Zou M et al (2015) Properties and structures of commercial polygalacturonase with ultrasound treatment: Role of ultrasound in enzyme activation. RSC Adv 5:107591–107600. https://doi.org/10.1039/c5ra19425c
Mohiddin FA, Padder SA, Baht AH et al (2021) Phylogeny and optimization of Trichoderma harzianum for chitinase production: evaluation of their antifungal behaviour against the prominent soil borne phyto-pathogens of temperate India. Microorganisms 9:1962. https://doi.org/10.3390/microorganisms9091962
Monks LM, Rigo A, Mazutti MA et al (2013) Use of chemical, enzymatic and ultrasound-assisted methods for cell disruption to obtain carotenoids. Biocatal Agric Biotechnol 2:165–169. https://doi.org/10.1016/j.bcab.2013.03.004
Nampoothiri KM, Baiju TV, Sandhya C et al (2004) Process optimization for antifungal chitinase production by Trichoderma harzianum. Process Biochem 39:1583–1590. https://doi.org/10.1016/S0032-9592(03)00282-6
Nitayavardhana S, Shrestha P, Rasmussen ML et al (2010) Ultrasound improved ethanol fermentation from cassava chips in cassava-based ethanol plants. Bioresour Technol 101:2741–2747. https://doi.org/10.1016/j.biortech.2009.10.075
Pandey A (1992) Recent process developments in solid-state fermentation. Process Biochem 27:109–117. https://doi.org/10.1016/0032-9592(92)80017-W
Pandey A (2003) Solid-state fermentation. Biochem Eng J 13:81–84. https://doi.org/10.1007/978-3-319-10464-5_10
Patil NS, Jadhav JP (2014) Enzymatic production of N-acetyl-d-glucosamine by solid state fermentation of chitinase by Penicillium ochrochloron MTCC 517 using agricultural residues. Int Biodeterior Biodegrad 91:9–17. https://doi.org/10.1016/j.ibiod.2014.03.003
Patil RS, Joshi SM, Gogate PR (2019) Intensification of delignification of sawdust and subsequent enzymatic hydrolysis using ultrasound. Ultrason Sonochem 58:1–9. https://doi.org/10.1016/j.ultsonch.2019.104656
Pawar SV, Rathod VK (2018) Ultrasound assisted process intensification of uricase and alkaline protease enzyme co-production in Bacillus licheniformis. Ultrason Sonochem 45:173–179. https://doi.org/10.1016/j.ultsonch.2018.03.004
Pereira RN, Vicente AA (2010) Environmental impact of novel thermal and non-thermal technologies in food processing. Food Res Int 43:1936–1943. https://doi.org/10.1016/j.foodres.2009.09.013
Pitt WG, Ross SA (2003) Ultrasound increases the rate of bacterial cell growth. Biotechnol Prog 19:1038–1044. https://doi.org/10.1021/bp0340685
Rachmawaty HP, Hartati ZM, Madihah MS (2019) Optimization of chitinase production by Trichoderma virens in solid state fermentation using response surface methodology. Mater Sci Forum 967:132–142. https://doi.org/10.4028/www.scientific.net/MSF.967.132
Rustiguel C, Jorge J, Guimarães L (2012) Optimization of the chitinase production by different Metarhizium anisopliae strains under solid-state fermentation with silkworm chrysalis as substrate using CCRD. Adv Microbiol 02:268–276. https://doi.org/10.4236/aim.2012.23032
Sakthiselvan P, Naveena B, Partha N (2012) Effect of medium composition and ultrasonication on xylanase production by Trichoderma harzianum MTCC 4358 on novel substrate. Afr J Biotechnol 11:12067–12077. https://doi.org/10.5897/ajb11.4301
Sallet D, Souza PO, Fischer LT et al (2019) Ultrasound-assisted extraction of lipids from Mortierella isabellina. J Food Eng 242:1–7. https://doi.org/10.1016/j.jfoodeng.2018.08.015
Schmaltz S, Aita BC, Alves EA et al (2021) Ultrasound-assisted fermentation for production of β-1,3-glucanase and chitinase by Beauveria bassiana. J Chem Technol Biotechnol 96:88–98. https://doi.org/10.1002/jctb.6514
Souza M, Mezadri ET, Zimmerman E et al (2013) Evaluation of activity of a commercial amylase under ultrasound-assisted irradiation. Ultrason Sonochem 20:89–94. https://doi.org/10.1016/j.ultsonch.2012.05.012
Steudler S, Werner A, Walther T (2019) It is the mix that matters: substrate-specific enzyme production from filamentous fungi and bacteria through solid-state fermentation. Solid state fermentation. Springer, pp 51–81
Sulaiman AZ, Ajit A, Yunus RM, Chisti Y (2011) Ultrasound-assisted fermentation enhances bioethanol productivity. Biochem Eng J 54:141–150. https://doi.org/10.1016/j.bej.2011.01.006
Valente IL, Confortin TC, Luft L et al (2020) Efects of ultrasound on submerged fermentation for producing antioxidant metabolites from Botryosphaeria dothidea. Braz J Chem Eng 37:475–484. https://doi.org/10.1007/s43153-020-00044-8
Vega FE, Goettel MS, Blackwell M et al (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159. https://doi.org/10.1016/j.funeco.2009.05.001
Wang Z, Lin X, Li P et al (2012) Effects of low intensity ultrasound on cellulase pretreatment. Bioresour Technol 117:222–227. https://doi.org/10.1016/j.biortech.2012.04.015
Wang F, Ma AZ, Guo C et al (2013) Ultrasound-intensified laccase production from Trametes versicolor. Ultrason Sonochem 20:118–124. https://doi.org/10.1016/j.ultsonch.2012.05.003
Acknowledgements
The authors thank the Research Support Foundation of the State of Rio Grande do Sul (FAPERGS: 17/2551-0000893-6) and National Council for Scientific and Technological Development (CNPq: 302579/2019-2) for the financial support. G.L. Zabot, M.V. Tres, R.C. Kuhn and M.A. Mazutti thank CNPq for the productivity grants.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no commercial or financial conflict of interest.
Rights and permissions
About this article
Cite this article
Mezadri, E.T., Kuhn, K.R., Schmaltz, S. et al. Evaluation of ultrasound waves for the production of chitinase and β-1,3 glucanase by Trichoderma harzianum through SSF. 3 Biotech 12, 122 (2022). https://doi.org/10.1007/s13205-022-03179-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-022-03179-2