Abstract
Purpose
Penicillium roqueforti ATCC 10110 was cultivated in rice husk residue, to produce a multienzymatic extract, which was characterised for its potential biotechnological applications.
Methods
Optimisation of the fermentation conditions for the xylanase activity production (U/g) was evaluated by using a Doehlert-type experimental design.
Results
The optimum xylanase activity (at 32 °C/82 h), was 1.04 U/g, which represented a deviation of 3% from the theoretically optimised value predicted by the quadratic model (R2 = 0.92). The optimum conditions were observed at pH 7.0 and 35 °C. The xylanase activity was favoured, particularly, by the presence (1 M) of Co2+ and Cu2+ and the kinetic constants were determined (K m = 7.22 mg/ml and v max = 3.29 U/g). For the endoglucanase activity, it was not possible to adjust a quadratic model but maximal activities (2.37 ± 0.01 U/g) were obtained at 32 °C for 72 h. For this enzyme, the optimum conditions were pH 4.8 and 50 °C. Also, Co2+, Cu2+, acetone, ethanol and isopropanol increased the endoglucanase activity.
Conclusion
The substrate rice husk, without any additives, permitted the acquisition of xylanases and endoglucanases similar to those obtained from synthetic substrates, justifying its application as a substrate for solid-state fermentations.
Similar content being viewed by others
References
Asgher, M., Wahab, A., Bilal, M., Iqbal, H.M.I.: Lignocellulose degradation and production of lignin modifying enzymes by Schizophyllum commune IBL-06 in solid-state fermentation. Biocatal. Agric. Biotechnol. (2016). doi:10.1016/j.bcab.2016.04.003
Bilal, M., Asgher, M., Shahida, M., Bhatti, H.N.: Characteristic features and dye degrading capability of agar–agar gel immobilized manganese peroxidase. Int. J. Biol. Macromol. (2016). doi:10.1016/j.ijbiomac.2016.02.014
Ajala, A.S., Gana, A.: Analysis of challenges facing rice processing in Nigeria. J. Food Process. (2015). doi:10.1155/2015/893673
Saha, B., Cotta, M.: Lime pretreatment, enzymatic saccharification and fermentation of rice hulls to ethanol. Biomass Bioenergy (2008). doi:10.1016/j.biombioe.2008.01.014
Cen, P., Xia, L.: Production of cellulase by solid-state fermentation. Adv. Biochem. Eng. Biotechnol. 65, 70–92 (1999)
Bilal, M., Asgher, M., Iqbal, H.M.N., Ramzan, M.: Enhanced bio-ethanol production from old newspapers waste through alkali and enzymatic delignification. Waste Biomass Valor. (2017) doi:10.1007/s12649-017-9871-7
Shraddha, S.R., Sehgal, S., Kamthania, M., Kumar, A.: Laccase: microbial sources, production, purification, and potential biotechnological applications. Enzyme Res. (2011). doi:10.4061/2011/217861
Singhania, R.R., Patel, A.K., Soccol, C.R., Pandey, A.: Recent advances in solid-state fermentation. J. Biochem. Eng. (2009). doi:10.1016/j.bej.2008.10.019
Pandey, A.: Solid-state fermentation. J. Biochem. Eng. (2003). doi:10.1016/S1369-703X(02)00121-3
Santos, T.C., Cavalcanti, I.S., Bonomo, R.C.F., Santana, N.B., Franco, M.: Optimization of productions of cellulolytic enzymes by Aspergillus niger using residue of mango a substrate. Ciencia Rural (2011). doi:10.1590/S0103-84782011005000145
Kalai, S., Anzala, L., Bensoussan, M., Dantigny, P.: Modelling the effect of temperature, pH, water activity, and organic acids on the germination time of Penicillium camemberti and Penicillium roqueforti conidia. Int J. Food Microbiol. (2016). doi:10.1016/j.ijfoodmicro.2016.03.024
Coughlan, M.P., Hazlewood, G.: β-1,4-d-Xylan-degrading enzyme systems: biochemistry, molecular biology and applications. Biotechnol. Appl. Biochem. (1993). doi:10.1111/j.1470-8744.1993.tb00244.x
Subramaniyan, S., Prema, P.: Biotechnology of microbial xylanases: enzymology, molecular biology and application. Crit. Rev. Biotechnol. 22(1), 33–46 (2002)
Camacho, N.A., Aguiar, O.G.: Production, purification and characterization of a low molecular mass xylanase from Aspergillus sp and it is application in bakery. Appl. Biochem. Biotechnol. (2003). doi:10.1385/ABAB:104:3:159
Prade, R.A.: Xylanases from biology to biotechnology. Biotechnol. Genet. Eng. Rev. (1995). doi:10.1080/02648725.1996.10647925
Hu, J., Arantes, V., Pribowo, A., Saddler, J.N.: The synergistic action of accessory enzymes enhances the hydrolytic potential of a “cellulase mixture” but is highly substrate specific. Biotechnol. Biofuels (2013). doi:10.1186/1754-6834-6-112
Rodrigues, M.I., Iemma, A.F.: Experimental Design and Process Optimization. CRC Press, Boca Raton (2014)
Mustafa, S.R., Husaini, A., Hipolito, C.N., Hussain, H., Suhaili, N.: Application of response surface methodology for optimizing process parameters in the production of amylase by Aspergillus flavus NSH9 under solid state fermentation. Braz. Arch. Biol. Biotechol. (2016). doi:10.1590/1678-4324-2016150632
dos Santos, T.C., Gomes, D.P.P., Bonomo, R.C.F., Franco, M.: Optimisation of solid state fermentation of potato peel for the production of cellulolytic enzymes. Food Chem. (2012). doi:10.1016/j.foodchem.2011.11.115
Santos, T.C., Filho, G.A., Oliveira, A.C., Rocha, T.J.O., Machado, F.P.P., Bonomo, R.C.F., Mota, K.I.A., Franco, M.: Application of response surface methodology for producing cellulolytic enzymes by solid-state fermentation from the puple mombin (Spondias purpurea L.) Residue. Food Sci. Biotechnol. (2013). doi:10.1007/s10068-013-0001-4
Miller, G.L.: Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. (1959). doi:10.1021/ac60147a030
Silva, L.A.O., Terrasan, C.R.F., Carmona, E.C.: Purification and characterization of xylanases from Trichoderma inhamatum. Electron. J. Biotechnol. (2015). doi:10.1016/j.ejbt.2015.06.001
Masutti, D.C., Borgognone, A., Setti, L.: Production of enzymes from rice husks and wheat straw in solid state fermentation. Chem. Eng. Trans. (2012). doi:10.3303/CET1227023
Arulanandham, T.V., Palaniswamy, M.: Production of xylanase by Penicillium frequentans isolated from litter soil using paddy straw as substrate by solid state fermentation. World J. Pharm. Pharm. Sci. (2016). doi:10.20959/wjpps201610-7763
Hedge, A., Ramesh, C.: Isolation and screening of fungi for the production of xylanase using solid-state fermentation from Sirsi region of Western Ghats of Karnataka, India. Int. J. Microbiol. (2016). doi:10.20546/ijcmas.2016.502.062
Pericin, D., Madarev-Popovic, S., Radulovi-Popovic L., Skrinjar M.: Evaluate of pumpkin oil cake as substrate for the cellulase production by Penicillium roqueforti in solid state fermentation. Rom. Biotechnol. Lett. 13(4), 3815–3820 (2008)
Khandeparkar, R.D.S., Bhosle, N.B.: Purification and characterization of Thermoalkalophilic xylanase isolated from the Enterobacter sp MTCC 5112. Res. Microbiol. (2006). doi:10.1016/j.resmic.2005.12.001
Knob, A., Carmona, C.C.: Xylanase production by Penicillium sclerotiorum and its characterization. World Appl. Sci. J. 4(2), 277–283 (2008)
Terrasan, C.R.F., Guisan, J.M., Carmona, E.C.: Xylanase and β-xylosidase from Penicillium janczewskii: purification, characterization and hydrolysis of substrates. Electron. J. Biotechnol. (2016). doi:10.1016/j.ejbt.2016.08.001
Querido, A.L.S., Coelho, J.L.C., Araújo, E.F., Chaves-Alves V.M.: Partial purification and characterization of xylanase produced by Penicillium expansum. Braz. Arch. Biol. Technol. (2006) doi:10.1590/S1516-89132006000400016
Saha, S.P., Ghosh, S.: Optimization of xylanase production by Penicillium citrinum xym2 and application in saccharification of agro-residues. Biocatal. Agric. Biotechnol. (2014). doi:10.1016/j.bcab.2014.03.003
Boonrung, S., Katekaew, S., Mongkolthanaruk, W., Aimi, T., Boonlue, S.: Purification and characterization of low molecular weight extreme alkaline xylanase from the thermophilic fungus Myceliophthora thermophila BF1-7. Myconscience (2016). doi:10.1016/j.myc.2016.07.003
Silva, V.C.T., Coto, A.L.S., Souza, R.C., Neves, M.B.S., Gomes, E., Bonilla-Rodriguez, G.O.: Effect of pH, temperature, and chemicals on the endoglucanases and β-glucosidases from the thermophilic fungus Myceliophthora heterothallica F.2.1.4. obtained by solid-state and submerged cultivation. Biochem. Res. Int. (2016). doi:10.1155/2016/9781216.
Azzeddine, B., Abdelaziz, M., Estelle, C., Mouloud, K., Nawel, B., Nabila, B., Francis, D., Said, B.: Optimization and partial characterization of endoglucanase produced by Streptomyces sp. B-png23. Arch. Biol. Sci. (2013). doi:10.2298/abs1302549a
Lin, L., Liu, X., Zhou, Y., Guan, L., He, J., Huang, W.: A novel pH-stable, endoglucanase (JqCel5A) isolated from a salt-lake microorganism, Jonesia quinghaiensis. Electron. J. Biotechnol. (2016). doi:10.1016/j.ejbt.2016.09.004
Das, A., Ghosh, U., Mohapatra, P.K.D., Pati, B.R., Mondal, K.C.: Study on thermodynamics and adsorption kinetics of purified endoglucanase (Endoglucanases) from Penicillium notatum NCIM NO-923 produced under mixed solid-state fermentation of waste cabbage and Bagasse. Braz. J. Microbiol. (2012). doi:10.1590/S1517-83822012000300037
Huang, S., Deng, G., Yang, Y., Wu, Z., Wu, L.: Optimization of Endoglucanase production from a novel bacterial isolate, Arthrobacter sp. HPG166 and characterization of its properties. Braz. Arch. Biol. Technol. (2015). doi:10.1590/S1516-89132015050256
Boonchuay, P., Takenaka, S., Kuntiya, A., Techapun, C., Leksawasdi, N., Seesuriyachan, P., Chaiyaso, T.: Purification, characterization, and molecular cloning of the xylanase from Streptomyces thermovulgaris TISTR1948 and its application to xylooligosaccharide production. J. Mol. Catal. B (2016). doi:10.1016/j.molcatb.2016.03.014
Asgher, M., Ramzan, M., Bilal, M.: Purification and characterization of manganese peroxidases from native and mutant Trametes versicolor IBL-04. Chin. J. Catal. 37, 561–570, (2016). doi:10.1016/S1872-2067(15)61044-0
Guan, G.Q., Zhao, P.X., Zhao, J., Wang, M.J., Huo, S.H., Cui, F.J., Jiang, J.X.: Production and partial characterization of an alkaline xylanase from a novel fungus Cladosporium oxysporum. BioMed Res. Int. (2016). doi:10.1155/2016/4575024
Burgess, R.R.: Protein precipitation techniques. Methods Enzymol. (2009). doi:10.1016/S0076-6879(09)63020-2
Moteshafi, H., Hashemi, M., Mousavi, S.M., Mousivand, M.: Characterization of produced xylanase by Bacillus subtilis D3d newly isolated from apricot phyllosphere and its potential in pre-digestion of BSG. J. Ind. Eng. Chem. (2016). doi:10.1016/j.jiec.2016.03.036
Sharma, P., Woldesenbet, F., Gupta, N.: Statistical optimization of the production of a cellulase-free, thermoalkali-stable, salt- and solvent-tolerant xylanase from Bacillus halodurans by solid-state fermentation. Arch. Appl. Sci. Res. 4(1), 524–535 (2012)
Sorgatto, M., Guimarães, N.C.A., Zanoelo, F.F., Marques, M.R., Peixoto-Nogueira, S.C., Giannesi, G.G.: Purification and characterization of an extracellular xylanase produced by the endophytic fungus Aspergillus terreus grown in submerged fermentation. Afri. J. Biotechnol. (2012). doi:10.5897/AJB11.2686
Sanghvi, G., Jivrajani, M., Patel, N., Jivrajani, H., Bhaskara, G.B., Patel, S.: Purification and characterization of haloalkaline, organic solvent stable xylanase from newly isolated halophilic bacterium-OKH. Int. Sch. Res. Not. (2014). doi:10.1155/2014/198251
Pol, D., Laxman, R.S., Rao, M.: Purification and biochemical characterization of endoglucanase from Penicillium pinophilum MS 20. Indian J. Biochem. Biophys. 49(3), 189–194 (2012)
Sadhu, S., Saha, P., Ken, S.K., Mayilraj, S., Maiti, T.K.: Production, purification and characterization of a novel thermotolerant endoglucanase (CMCase) from Bacillus strain isolated from cow dung. Springer Plus (2013). doi:10.1186/2193-1801-2-10
Liao, H., Zheng, H., Li, S., Wei, Z., Mei, X., Ma, H., Shen, Q., Xu, Y.: Functional diversity and properties of multiple xylanases from Penicillium oxalicum GZ-2. Sci. Rep. (2015). doi:10.1038/srep12631
Chutani, P., Sharma, K.K.: Biochemical evaluation of xylanases from various filamentous fungi and their application for the deinking of ozone treated newspaper pulp. Carbohydr. Polym. (2015). doi:10.1016/j.carbpol.2015.03.053
Acknowledgements
Authors would like to acknowledge the Banco do Nordeste do Brasil (BNB, Brazil), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil), the Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) for their important financial support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Marques, G.L., dos Santos Reis, N., Silva, T.P. et al. Production and Characterisation of Xylanase and Endoglucanases Produced by Penicillium roqueforti ATCC 10110 Through the Solid-State Fermentation of Rice Husk Residue. Waste Biomass Valor 9, 2061–2069 (2018). https://doi.org/10.1007/s12649-017-9994-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12649-017-9994-x