Skip to main content
SpringerLink
Log in

Application of Chemometric Methods for the Optimization Secretion of Xylanase by Aspergillus oryzae in Solid State Fermentation and Its Application in the Saccharification of Agro-industrial Waste

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

Abstract

In the present work, a complete study of the production of xylanase by solid-state fermentation (SSF) on a residue mixture by the fungus Aspergillus oryzae ATCC 10124 was conducted, examining the optimization of enzyme production, its physicochemical characterization and saccharification. For optimization of enzyme production, two statistical designs were applied to optimize the mixture of waste residues and fermentation parameters. The centroid simplex experimental design was applied to identify the best composition of residues, sugarcane bagasse (SB), rice husk (RS) and cocoa bean shell (CS) demonstrating that a combination of 25% SB, 25% RS and 50% CS was optimal. Box–Behnken experimental design was applied to optimize fermentation factors, humidity, time and temperature, demonstrating that the combination of 55% humidity, 100 h and 25 °C was the most effective for obtaining high enzyme titers. After both optimizations, an increase of up to 165% in enzymatic activity was observed compared to non-optimized production. The xylanase produced in this fermentation process showed alkaline characteristics and high thermal stability. The multienzyme extract (ME) was applied directly for the saccharification of agro-industrial residues with satisfactory results for all lignocellulosic residues tested: sugarcane bagasse, rice husk, cocoa husk and peanut husk, highlighting the possibility of a one-step reduction in the enzymatic process. The saccharification using the ME was efficient, without the need for the enzyme purification step.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

The collected data can be handed out upon request.

Abbreviations

BBD:

Box–Behnken Design

CS:

Cocoa bean shell

Df:

Degrees of freedom

DS:

Dried solids

MD:

Mixture design

ME:

Multienzyme extract

ME:

Multienzyme extract

MS:

Mean squares

PDA:

Potato-dextrose-agar

RS:

Rice husk

RSM:

Response surface methodology

SB:

Sugarcane bagasse

SD:

Standard deviation

SS:

Sum of squares

SSF:

Solid-state fermentation

References

  1. Garcia, D.J., Lovett, B.M., You, F.: Considering agricultural wastes and ecosystem servicesin food-energy-water-waste nexus system design. J. Clean. Prod. (2019). https://doi.org/10.1016/j.jclepro.2019.04.314

    Article  Google Scholar 

  2. Hashemi, S.S., Karimi, K., Majid Karimi, A.: Ethanolic ammonia pretreatment for efficient biogas production from sugarcane bagasse. Fuel (2019). https://doi.org/10.1016/j.fuel.2019.03.080

    Article  Google Scholar 

  3. Vásquez, Z.S., de Carvalho Neto, D.P., Pereira, G.V.M., Vandenberghe, L.P.S., de Oliveira, P.Z., Tiburcio, P.B., Rogez, H.L.G., Góes Neto, A., Soccol, C.R.: Biotechnological approaches for cocoa waste management: a review. Waste Manag. (2019). https://doi.org/10.1016/j.wasman.2019.04.030

    Article  Google Scholar 

  4. Brito, A.R., dos Santos Reis, N., Silva, T.P., Ferreira Bonomo, R.C., Uetanabaro, A.P.T., de Assis, S.A., da Silva, E.G.P., Aguiar-Oliveira, E., Oliveira, J.R., Franco, M.: Comparison between the univariate and multivariate analysis on the partial characterization of the endoglucanase produced in the solid state fermentation by Aspergillus oryzae ATCC 10124. Prep. Biochem. Biotechnol. (2017). https://doi.org/10.1080/10826068.2017.1365247

    Article  Google Scholar 

  5. Souza, L.O., de Brito, A.R., Bonomo, R.C.F., Santana, N.B., de Almeida Antunes Ferraz, J.L., Aguiar-Oliveira, E., de Araújo Fernandes, A.G., Ferreira, M.L.O., de Oliveira, J.R., Franco, M.: Comparison of the biochemical properties between the xylanases of Thermomyces lanuginosus (Sigma®) and excreted by Penicillium roqueforti ATCC 10110 during the solid state fermentation of sugarcane bagasse. Biocatal. Agric. Biotechnol. (2018). https://doi.org/10.1016/j.bcab.2018.08.016

    Article  Google Scholar 

  6. Soares, G.A., Alnoch, R.C., Silva Dias, G., dos Santos Reis, N., de Carvalho Tavares, I.M., Ruiz, H.A., Bilal, M., Oliveira, J.R., Krienger, N., Franco, M.: Production of fermented solid containing lipases from Penicillium roqueforti ATCC 10110 and its direct employment in organic medium in ethyl Oleate synthesis. Biotechnol. Appl. Biochem. (2021). https://doi.org/10.1002/bab.2202

    Article  Google Scholar 

  7. dos Santos Reis, N., Lessa, O.A., Pacheco, C.S.V., Pereira, N.E., Soares, G.A., Silva, E.G.P., Oliveira, J.R., Franco, M.: Cocoa shell as a substrate for obtaining endoglucanase and xylanase from Aspergillus oryzae ATCC 10124. Acta. Sci. Technol. (2020). https://doi.org/10.4025/actascitechnol.v42i1.48211

    Article  Google Scholar 

  8. Oliveira, P.C., de Brito, A.R., Pimentel, A.B., Soares, G.A., Pacheco, C.S.V., Santana, N.B., da Silva, E.G.P., Fernandes, A.G.A., Ferreira, M.L.O., de Oliveira, J.R., Franco, M.: Cocoa shell for the production of endoglucanase by Penicillium roqueforti ATCC 10110 in solid state fermentation and biochemical properties. Rev. Mex. Ing. Quim. (2019). https://doi.org/10.24275/uam/izt/dcbi/revmexingquim/2019v18n3/Oliveira

    Article  Google Scholar 

  9. da SilvaNunes, N., Carneiro, L.L., de Menezes, L.H.S., de Carvalho, M.S., Pimentel, A.B., Silva, T.P., Pacheco, C.S.V., de CarvalhoTavares, I.M., Santos, P.H., dos Chagas, T.P., da Silva, E.G.P., de Oliveira, J.R., Bilal, M., Franco, M.: Simplex-centroid design and artificial neural network-genetic algorithm for the optimization of exoglucanase production by Penicillium Roqueforti ATCC 10110 through solid-state fermentation using a blend of Agroindustrial Wastes. BioEnergy Res. (2020). https://doi.org/10.1007/s12155-020-10157-0

    Article  Google Scholar 

  10. das Neves, C.A.A., de Menezes, L.H.S.H.S., Soares, G.A.A., Reis, N., Dos, S., Tavares, I.M.C., Franco, M., de Oliveira, J.R.R.: Production and biochemical characterization of halotolerant β-glucosidase by Penicillium roqueforti ATCC 10110 grown in forage palm under solid-state fermentation. Biomass Convers. Biorefinery. (2020). https://doi.org/10.1007/s13399-020-00930-8

    Article  Google Scholar 

  11. Nogueira, L.S., Tavares, I.M.C., Santana, N.B., Ferrão, S.P.B., Teixeira, J.M., Costa, F.S., Silva, T.P., Pereira, H.J.V., Irfan, M., de Bilal, M., Oliveira, J.R.R., Franco, M.: Thermostable trypsin-like protease by Penicillium roqueforti secreted in cocoa shell fermentation: production optimization, characterization, and application in milk clotting. Biotechnol. Appl. Biochem. (2021). https://doi.org/10.1002/bab.2268

    Article  Google Scholar 

  12. Ezeilo, U.R., Lee, C.T., Huyop, F., Zakaria, I.I., Wahab, R.A.: Raw oil palm frond leaves as cost-effective substrate for cellulase and xylanase productions by Trichoderma asperellum UC1 under solid-state fermentation. J. Environ. Manage. (2019). https://doi.org/10.1016/j.jenvman.2019.04.113

    Article  Google Scholar 

  13. de Almeida Antunes Ferraz, J.L., Souza, L.O., de Araújo Fernandes, A.G., Oliveira, M.L.F., de Oliveira, J.R., Franco, M.: Optimization of the solid-state fermentation conditions and characterization of xylanase produced by Penicillium roqueforti ATCC 10110 using yellow mombin residue (Spondias mombin L.). Chem. Eng. Commun. (2020). https://doi.org/10.1080/00986445.2019.1572000

    Article  Google Scholar 

  14. Rodríguez, P., Cerda, A., Font, X., Sánchez, A., Artola, A.: Valorisation of biowaste digestate through solid state fermentation to produce biopesticides from Bacillus thuringiensis. Waste Manag. (2019). https://doi.org/10.1016/j.wasman.2019.05.026

    Article  Google Scholar 

  15. Sadh, P.K., Duhan, S., Duhan, J.S.: Agro-industrial wastes and their utilization using solid state fermentation: a review. Bioresour. Bioprocess. (2018). https://doi.org/10.1186/s40643-017-0187-z

    Article  Google Scholar 

  16. Costa, J.A.V., Treichel, H., Kumar, V., Pandey, A.: Advances in Solid-State Fermentation. In: Current Developments in Biotechnology and Bioengineering. Elsevier (2018).

  17. de Santos, T.C., Diniz, G.A., De Brito, A.R., Pires, A.J.V., Franco, M.: Effect of solid state fermentation on nutritional content and evaluation of degradability in cactus pear. Rev. Caatinga (2015). https://doi.org/10.1590/1983-21252015v28n328rc

    Article  Google Scholar 

  18. dos Santos, T.C., Abreu Filho, G., De Brito, A.R., Pires, A.J.V., Bonomo, R.C.F., Franco, M.: Production and characterization of cellulolytic enzymes by Aspergillus niger and Rhizopus sp. by solid state fermentation of prickly pear. Rev. Caatinga (2016). https://doi.org/10.1590/1983-21252016v29n126rc

    Article  Google Scholar 

  19. Lessa, O.A., dos Santos Reis, N., Leite, S.G.F., Gutarra, M.L.E., Souza, A.O., Gualberto, S.A., de Oliveira, J.R., Aguiar-Oliveira, E., Franco, M.: Effect of the solid state fermentation of cocoa shell on the secondary metabolites, antioxidant activity, and fatty acids. Food Sci. Biotechnol. (2018). https://doi.org/10.1007/s10068-017-0196-x

    Article  Google Scholar 

  20. Nalini, S., Parthasarathi, R.: Optimization of rhamnolipid biosurfactant production from Serratia rubidaea SNAU02 under solid-state fermentation and its biocontrol efficacy against Fusarium wilt of eggplant. Ann. Agrar. Sci. (2018). https://doi.org/10.1016/j.aasci.2017.11.002

    Article  Google Scholar 

  21. Intasit, R., Cheirsilp, B., Louhasakul, Y., Boonsawang, P., Chaiprapat, S., Yeesang, J.: Valorization of palm biomass wastes for biodiesel feedstock and clean solid biofuel through non-sterile repeated solid-state fermentation. Bioresour. Technol. (2020). https://doi.org/10.1016/j.biortech.2019.122551

    Article  Google Scholar 

  22. Sala, A., Artola, A., Sánchez, A., Barrena, R.: Rice husk as a source for fungal biopesticide production by solid-state fermentation using B. bassiana and T. harzianum. Bioresour. Technol. (2020). https://doi.org/10.1016/j.biortech.2019.122322

    Article  Google Scholar 

  23. de Menezes, L.H.S., Carneiro, L.L., Tavares, I.M., de Carvalho, T., Santos, P.H., das Chagas, T.P., Mendes, A.A., da Silva, E.G.P., Franco, M., de Oliveira, J.R.: Artificial neural network hybridized with a genetic algorithm for optimization of lipase production from Penicillium roqueforti ATCC 10110 in solid-state fermentation. Biocatal. Agric. Biotechnol. (2021). https://doi.org/10.1016/j.bcab.2020.101885

    Article  Google Scholar 

  24. Silva, T.P., Souza, L.O., Reis, N.S., Assis, S.A., Ferreira, M.L.O., de Oliveira, J.R., Aguiar-Oliveira, E., Franco, M.: Cultivation of Penicillium roqueforti in cocoa shell to produce and characterize its lipase extract. Rev. Mex. Ing. Quim. 16, 745–756 (2017)

    Google Scholar 

  25. Irfan, M., Asghar, U., Nadeem, M., Nelofer, R., Syed, Q., Shakir, H.A., Qazi, J.I.: Statistical optimization of saccharification of alkali pretreated wheat straw for bioethanol production. Waste Biomass Valorization (2016). https://doi.org/10.1007/s12649-016-9540-2

    Article  Google Scholar 

  26. Gupta, P.K., Choudhary, S., Chandrananthi, C., Sharon Eveline, J., Sushmitha, S.P., Hiremath, L., Srivastava, A.K., Narendra Kumar, S.: Fungal Biodiversity Producing Xylanase Enzymes Involved in Efficient Uses of Xylanolysis. In: Naraian, R. (ed.) Mycodegradation of Lignocelluloses. Springer, Cham (2019)

    Google Scholar 

  27. Ang, S.K., Shaza, E.M., Adibah, Y., Suraini, A.A., Madihah, M.S.: Production of cellulases and xylanase by Aspergillus fumigatus SK1 using untreated oil palm trunk through solid state fermentation. Process Biochem. (2013). https://doi.org/10.1016/j.procbio.2013.06.019

    Article  Google Scholar 

  28. Amin, M., Bhatti, H.N., Sadaf, S., Bilal, M.: Enhancing Lipase Biosynthesis by Aspergillus Melleus and its biocatalytic potential for degradation of polyester Vylon-200. Catal Lett (2021). https://doi.org/10.1007/s10562-020-03476-6

    Article  Google Scholar 

  29. Menezes, L.H.S., Carneiro, L.L., de Carvalho Tavares, I.M., Santos, P.H., Chagas, T.P., Mendes, A.A., Silva, E.G.P., Franco, M., de Oliveira, J.R.: Artificial neural network hybridized with a genetic algorithm for optimization of lipase production from Penicillium roqueforti ATCC 10110 in solid-state fermentation. Biocatal. Agric. Biotechnol. (2021). https://doi.org/10.1016/j.bcab.2020.101885

    Article  Google Scholar 

  30. Filipe, D., Fernandes, H., Castro, C., Peres, H., Oliva-Teles, A., Belo, I., Salgado, J.M.: Improved lignocellulolytic enzyme production and antioxidant extraction using solid-state fermentation of olive pomace mixed with winery waste. Biofuels Bioprod. Biorefining (2020). https://doi.org/10.1002/bbb.2073

    Article  Google Scholar 

  31. Box, G.E.P., Hunter, W.G., Hunter, J.S.: Statistics for Experimenters. Wiley, New York (1978)

    MATH  Google Scholar 

  32. Bezerra, M.A., Lemos, V.A., Novaes, C.G., de Jesus, R.M., Filho, H.R.S., Araújo, S.A., Alves, J.P.S.: Application of mixture design in analytical chemistry. Microchem. J. (2020). https://doi.org/10.1016/j.microc.2019.104336

    Article  Google Scholar 

  33. de Oliveira, R.L., da Silva, M.F., Converti, A., Porto, T.S.: Production of β-fructofuranosidase with transfructosylating activity by Aspergillus tamarii URM4634 Solid-State Fermentation on agroindustrial by-products. Int. J. Biol. Macromol. (2020). https://doi.org/10.1016/j.ijbiomac.2019.12.084

    Article  Google Scholar 

  34. Azcarate, S.M., Pinto, L., Goicoechea, H.C.: Applications of mixture experiments for response surface methodology implementation in analytical methods development. J. Chemom. (2020). https://doi.org/10.1002/cem.3246

    Article  Google Scholar 

  35. Ferreira, S.L.C., Bruns, R.E., Ferreira, H.S., Matos, G.D., David, J.M., Brandão, G.C., da Silva, E.G.P., Portugal, L.A., dos Reis, P.S., Souza, A.S., dos Santos, W.N.L.: Box-Behnken design: An alternative for the optimization of analytical methods. Anal. Chim. Acta (2007). https://doi.org/10.1016/j.aca.2007.07.011

    Article  Google Scholar 

  36. Ghose, T.K., Bisaria, V.S.: Measurement of hemicellulase activities: Part I Xylanases. Pure Appl. Chem. (1987). https://doi.org/10.1351/pac198759121739

    Article  Google Scholar 

  37. Miller, G.L.: Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar. Anal. Chem. (1959). https://doi.org/10.1021/ac60147a030

    Article  Google Scholar 

  38. Melnichuk, N., Braia, M.J., Anselmi, P.A., Meini, M.-R., Romanini, D.: Valorization of two agroindustrial wastes to produce alpha-amylase enzyme from Aspergillus oryzae by solid-state fermentation. Waste Manag. (2020). https://doi.org/10.1016/j.wasman.2020.03.025

    Article  Google Scholar 

  39. de Castro, R.J.S., Sato, H.H.: Synergistic effects of agroindustrial wastes on simultaneous production of protease and α-amylase under solid state fermentation using a simplex centroid mixture design. Ind. Crops Prod. (2013). https://doi.org/10.1016/j.indcrop.2013.07.002

    Article  Google Scholar 

  40. Bhardwaj, N., Verma, V.K., Chaturvedi, V., Verma, P.: Cloning, expression and characterization of a thermo-alkali-stable xylanase from Aspergillus oryzae LC1 in Escherichia coli BL21(DE3). Protein Expr. Purif. (2020). https://doi.org/10.1016/j.pep.2019.105551

    Article  Google Scholar 

  41. de Almeida Antunes, J.L., Souza, L.O., Soares, G.A., Coutinho, J.P., de Oliveira, J.R., Aguiar-Oliveira, E., Franco, M.: Enzymatic saccharification of lignocellulosic residues using cellulolytic enzyme extract produced by Penicillium roqueforti ATCC 10110 cultivated on residue of yellow mombin fruit. Bioresour. Technol. (2018). https://doi.org/10.1016/j.biortech.2017.06.048

    Article  Google Scholar 

  42. Bhardwaj, N., Kumar, B., Agarwal, K., Chaturvedi, V., Verma, P.: Purification and characterization of a thermo-acid/alkali stable xylanases from Aspergillus oryzae LC1 and its application in Xylo-oligosaccharides production from lignocellulosic agricultural wastes. Int. J. Biol. Macromol. (2019). https://doi.org/10.1016/j.ijbiomac.2018.09.070

    Article  Google Scholar 

  43. Kaur, A., Varghese, L.M., Mahajan, R.: Simultaneous production of industrially important alkaline xylanase-pectinase enzymes by a bacterium at low cost under solid-state fermentation conditions. Biotechnol Appl Biochem (2019). https://doi.org/10.1002/bab.1757

    Article  Google Scholar 

  44. Mukasekuru, M.R., Kaneza, P., Sun, H., Sun, F.F., He, J., Zheng, P.: Fed-batch high-solids enzymatic saccharification of lignocellulosic substrates with a combination of additives and accessory enzymes. Ind. Crops Prod. (2020). https://doi.org/10.1016/j.indcrop.2020.112156

    Article  Google Scholar 

  45. Prajapati, B.P., Jana, U.K., Suryawanshi, R.K., Kango, N.: Sugarcane bagasse saccharification using Aspergillus tubingensis enzymatic cocktail for 2G bio-ethanol production. Renew. Energy (2020). https://doi.org/10.1016/j.renene.2020.01.063

    Article  Google Scholar 

  46. Sharma, S., Bajaj, B.K.: Xylanase production from a new strain of Aspergillus terreus S9 and its application for saccharification of rice straw using combinatorial approach. Environ. Prog. Sustain. Energy (2018). https://doi.org/10.1002/ep.12779

    Article  Google Scholar 

Download references

Funding

The authors would like to thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico [308300/2021-1], and Fundação de Amparo à Pesquisa do Estado da Bahia for their financial support.

Author information

Authors and Affiliations

  1. Department of Exact Sciences and Technology, State University of Santa Cruz, Ilheus, 45654-370, Brazil

    Marise Silva de Carvalho, Julieta Rangel de Oliveira & Marcelo Franco

  2. Department of Biological Sciences, State University of Santa Cruz, Ilheus, 45654-370, Brazil

    Luiz Henrique Sales de Menezes, Adriana Bispo Pimentel & João Carlos Teixeira Dias

  3. Department of Chemistry, Federal University of Paraná, Curitiba, 81531-980, Brazil

    Floriatan Santos Costa

  4. Department of Exact Sciences and Natural, State University of Southwest Bahia, Itapetinga, 45700-000, Brazil

    Polyane Cabral Oliveira, Marta Maria Oliveira dos Santos & Iasnaia Maria de Carvalho Tavares

  5. Department of Biotechnology, Faculty of Science, University of Sargodha, Sargodha, 40100, Pakistan

    Muhammad Irfan

  6. School of Life Science and Food Engineering, Huaiyin Institute of Technology, Huaian, 223003, China

    Muhammad Bilal

Authors
  1. Marise Silva de Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luiz Henrique Sales de Menezes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adriana Bispo Pimentel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Floriatan Santos Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Polyane Cabral Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marta Maria Oliveira dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Iasnaia Maria de Carvalho Tavares
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Muhammad Irfan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Muhammad Bilal
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. João Carlos Teixeira Dias
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Julieta Rangel de Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Marcelo Franco
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marcelo Franco.

Ethics declarations

Competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Carvalho, M.S., de Menezes, L.H.S., Pimentel, A.B. et al. Application of Chemometric Methods for the Optimization Secretion of Xylanase by Aspergillus oryzae in Solid State Fermentation and Its Application in the Saccharification of Agro-industrial Waste. Waste Biomass Valor 14, 3183–3193 (2023). https://doi.org/10.1007/s12649-022-01832-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-022-01832-8

Keywords

Search

Navigation