Abstract
In Mexico, the generation of agave bagasse (AB) has increased considerably in recent years, given the growing global demand for tequila and other products from agave plants; around 45 thousand tons of AB are produced monthly only from tequila production. Despite the potential of AB to produce high-value metabolites, its use is limited. Several efforts have been made to mitigate the environmental problem caused by the final disposition of AB; however, the use of AB to produce enzymes has not been widely explored. This work presents a comparative analysis of the bioconversion of AB by Aspergillus fumigatus and Penicillium citrinum to produce cellulases and xylanases by solid-state fermentation, using wheat straw (WS) and sugarcane bagasse (SCB) as control feedstocks. The highest cellulase productions were obtained on AB with 10,112 and 7,347 U/kg of AB by P. citrinum and A. fumigatus, respectively. Regarding the xylanase production, the best producer was A. fumigatus (125,250 U/kg of WS), while the maximum xylanase production on AB was 28,974 U/kg of AB by P. citrinum. These results show the promising potential of AB to produce lignocellulase enzymes and open the vision towards implementing a circular economy strategy around the agave plant transformation.
Graphic Abstract
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included this published article and its supplementary information files.
References
Saldarriaga-Hernández, S., Velasco-Ayala, C., Leal-Isla Flores, P., de Jesús Rostro-Alanis, M., Parra-Saldivar, R., Iqbal, H.M.N., Carrillo-Nieves, D.: Biotransformation of lignocellulosic biomass into industrially relevant products with the aid of fungi-derived lignocellulolytic enzymes. Int. J. Biol. Macromol. 161, 1099–1116 (2020). Doi: https://doi.org/10.1016/j.ijbiomac.2020.06.047
Singh, R., Kumar, M., Mittal, A., Mehta, P.K.: Microbial enzymes: industrial progress in 21st century. 3 Biotech. 6, 1–15 (2016). Doi: https://doi.org/10.1007/s13205-016-0485-8
Peña-Maravilla, M., Calixto-Romo, M.A., Guillen-Navarro, K., Sanchez, J., Amaya-Delgado, L.: Cellulases and xylanases production by Penicillium citrinum CGETCR using coffee pulp in solid state fermentation. Rev. Mex. Ing. Química. 16, 757–769 (2017)
Silva-Mendoza, J., Gómez-Treviño, A., López-Chuken, U., Blanco-Gámez, E.A., Chávez-Guerrero, L., Cantú-Cárdenas, M.E.: Agave Leaves as a Substrate for the Production of Cellulases by Penicillium sp . and the Obtainment of Reducing Sugars . J. Chem. 2020, 1–7 (2020). Doi: https://doi.org/10.1155/2020/6092165
Sadh, P.K., Duhan, S., Duhan, J.S.: Agro-industrial wastes and their utilization using solid state fermentation: a review. Bioresour. Bioprocess. 5, 1–15 (2018). https://doi.org/10.1186/s40643-017-0187-z
Hernández, C., Escamilla-Alvarado, C., Sánchez, A., Alarcón, E., Ziarelli, F., Musule, R., Valdez-Vazquez, I.: Wheat straw, corn stover, sugarcane, and Agave biomasses: chemical properties, availability, and cellulosic-bioethanol production potential in Mexico. Biofuels, Bioprod. Biorefining. 13, 1143–1159 (2019). Doi: https://doi.org/10.1002/bbb.2017
Palomo-Briones, R., López-Gutiérrez, I., Islas-Lugo, F., Galindo-Hernández, K.L., Munguía-Aguilar, D., Rincón-Pérez, J.A., Cortés-Carmona, M.Á., Alatriste-Mondragón, F., Razo-Flores, E.: Agave bagasse biorefinery: processing and perspectives. Clean Technol. Environ. Policy. 20, 1423–1441 (2018). https://doi.org/10.1007/s10098-017-1421-2
Sanchez, A., Sanchez, S., Dueñas, P., Hernandez-Sanchez, P., Guadalajara, Y.: The role of sustainability analysis in the revalorization of Tequila residues and wastes using biorefineries. Waste Biomass Valorization 11, 701–713 (2020). https://doi.org/10.1007/s12649-019-00756-0
CRT: Consumo de Agave para tequila y tequila 100% de Agave. https://www.crt.org.mx/EstadisticasCRTweb/ (in Spanish) (2019). Accessed 26 September 2020
Bala, A., Singh, B.: Cellulolytic and xylanolytic enzymes of thermophiles for the production of renewable biofuels. Renew. Energy. 136, 1231–1244 (2019). https://doi.org/10.1016/j.renene.2018.09.100
Kumar, A., Rani, R., Pandey, A.: Chapter 2 - Production, Purification, and Application of Microbial Enzymes. In: Biotechnology of Microbial Enzymes. pp. 13–41. (2017)
Steudler, S., Werner, A., Walther, T.: It Is the Mix that Matters: Substrate-Specific Enzyme Production from Filamentous Fungi and Bacteria Through Solid-State Fermentation. In: Solid State Fermentation, pp. 51–81. Springer, Cham (2019)
Dai, J., Bean, B., Brown, B., Bruening, W., Edwards, J., Flowers, M., Karow, R., Lee, C., Morgan, G., Ottman, M., Ransom, J., Wiersma, J.: Harvest index and straw yield of five classes of wheat. Biomass Bioenerg. 85, 223–227 (2016). https://doi.org/10.1016/j.biombioe.2015.12.023
Townsend, T.J., Sparkes, D.L., Ramsden, S.J., Glithero, N.J., Wilson, P.: Wheat straw availability for bioenergy in England. Energy Policy. 122, 349–357 (2018). https://doi.org/10.1016/j.enpol.2018.07.053
Contreras-Hernández, M.G., Aréchiga-Carvajal, E.T., Moreno-Jiménez, M.R., González-Herrera, S.M., López-Miranda, J., Prado-Barragán, L.A., Rutiaga-Quiñones, O.M.: Enzymatic potential of native fungal strains of Agave residues. BioResources 13, 569–585 (2018). https://doi.org/10.15376/biores.13.1.569-585
Nava-Cruz, N.Y., Contreras-Esquivel, J.C., Aguilar-González, M.A., Nuncio, A., Rodríguez-Herrera, R., Aguilar, C.N.: Agave atrovirens fibers as substrate and support for solid-state fermentation for cellulase production by Trichoderma asperellum. 3 Biotech. 6, 115 (2016). https://doi.org/10.1007/s13205-016-0426-6
Barbosa, F.C., Silvello, M.A., Goldbeck, R.: Cellulase and oxidative enzymes: new approaches, challenges and perspectives on cellulose degradation for bioethanol production. Biotechnol. Lett. 42, 875–884 (2020). https://doi.org/10.1007/s10529-020-02875-4
Taherzadeh, A., Panahi, R., Mokhtarani, B.: Optimizing the combination of conventional carbonaceous additives of culture media to produce lignocellulose-degrading enzymes by Trichoderma reesei in solid state fermentation of agricultural residues. Renew. Energy. 131, 946–955 (2019). https://doi.org/10.1016/j.renene.2018.07.130
Molino, A., Larocca, V., Chianese, S., Musmarra, D.: Biofuels production by biomass gasification: a review. Energies. 11, 1–31 (2018). https://doi.org/10.3390/en11040811
Bagewadi, Z.K., Mulla, S.I., Shouche, Y., Ninnekar, H.Z.: Xylanase production from Penicillium citrinum isolate HZN13 using response surface methodology and characterization of immobilized xylanase on glutaraldehyde-activated calcium-alginate beads. 3 Biotech. 6, 1–18. (2016). https://doi.org/10.1007/s13205-016-0484-9
de Oliveira Rodrigues, P., dos Santos, B.V., Costa, L., Henrique, M.A., Pasquini, D., Baffi, M.A.: Xylanase and β-glucosidase production by Aspergillus fumigatus using commercial and lignocellulosic substrates submitted to chemical pre-treatments. Ind. Crops Prod. 95, 453–459 (2017). https://doi.org/10.1016/j.indcrop.2016.10.055
dos Santos, B.V., Rodrigues, P.O., Albuquerque, C.J.B., Pasquini, D., Baffi, M.A.: Use of an (Hemi) Cellulolytic Enzymatic Extract Produced by Aspergilli Species Consortium in the Saccharification of Biomass Sorghum. Appl. Biochem. Biotechnol. 189, 37–48 (2019). https://doi.org/10.1007/s12010-019-02991-6
Passos, D. de F., Pereira, N., Castro, A.M. de.: A comparative review of recent advances in cellulases production by Aspergillus, Penicillium and Trichoderma strains and their use for lignocellulose deconstruction. Curr. Opin. Green Sustain. Chem. 14, 60–66 (2018). https://doi.org/10.1016/j.cogsc.2018.06.003
Binod, P., Gnansounou, E., Sindhu, R., Pandey, A.: Enzymes for second generation biofuels: recent developments and future perspectives. Bioresour. Technol. Rep. 5, 317–325 (2019). https://doi.org/10.1016/j.biteb.2018.06.005
Gloster, T.: Exploitation of carbohydrate processing enzymes in biocatalysis. Curr. Opin. Chem. Biol. 55, 180–188 (2020). https://doi.org/10.1016/j.cbpa.2020.01.015
Olofsson, J., Barta, Z., Börjesson, P., Wallberg, O.: Integrating enzyme fermentation in lignocellulosic ethanol production: Life-cycle assessment and techno-economic analysis. Biotechnol. Biofuels 10, 1–14 (2017). https://doi.org/10.1186/s13068-017-0733-0
Walia, A., Guleria, S., Mehta, P., Chauhan, A., Parkash, J.: Microbial xylanases and their industrial application in pulp and paper biobleaching: a review. 3 Biotech. 7, 1–12. (2017). https://doi.org/10.1007/s13205-016-0584-6
Sluiter, A., Hames, B., Ruiz, R., Scarlata, C., Slui, J., ter, D. Templeton, and D.C.: Determination of Structural Carbohydrates and Lignin in Biomass. Laboratory Analytical Procedure (LAP). TP-510-42618 (2012).
Durand, A.: Bioreactor designs for solid state fermentation. Biochem. Eng. J. 13, 113–125 (2003). https://doi.org/10.1016/S1369-703X(02)00124-9
Perez-Pimienta, J.A., Lopez-Ortega, M.G., Chavez-Carvayar, J.A., Varanasi, P., Stavila, V., Cheng, G., Singh, S., Simmons, B.A.: Characterization of agave bagasse as a function ofionic liquid pretreatment. Biomass Bioenergy 75, 180–188 (2015). https://doi.org/10.1016/j.biombioe.2015.02.026
Rios-González, L.J., Morales-Martínez, T.K., Rodríguez-Flores, M.F., Rodríguez-De la Garza, J.A., Castillo-Quiroz, D., Castro-Montoya, A.J., Martinez, A.: Autohydrolysis pretreatment assessment in ethanol production from agave bagasse. Bioresour. Technol. 242, 184–190 (2017). https://doi.org/10.1016/j.biortech.2017.03.039
Akula, S., Golla, N.: Significance of process parameters on fungal cellulase production. In: Biofuel Production Technologies: Critical Analysis for Sustainability, pp. 299–324. Springer, Singapore (2020)
Khaleghian, H., Molaverdi, M., Karimi, K.: Silica removal from rice straw to improve its hydrolysis and ethanol production. Ind. Eng. Chem. Res. 56, 9793–9798 (2017). https://doi.org/10.1021/acs.iecr.7b02830
Salazar-Leyva, J.A., Osuna-Ruiz, I., Rodríguez-Tirado, V.A., Zazueta-Patrón, I.E., Brito-Rojas, H.D.: Optimization study of fructans extraction from Agave tequilana weber azul variety. Food Sci. Technol. 36, 631–637 (2016). https://doi.org/10.1590/1678-457X.11216
Rastegari, A.A.: Chapter 8—Molecular mechanism of cellulase production systems in Penicillium. In: New and Future Developments in Microbial Biotechnology and Bioengineering, pp. 153–166. Elsevier, Amsterdam (2018)
Kapoor, M., Panwar, D., Kaira, G.S.: Chapter 3—Bioprocesses for Enzyme Production Using Agro-Industrial Wastes: Technical Challenges and Commercialization Potential. In: Agro-Industrial Wastes as Feedstock for Enzyme Production, pp. 61–93. (2016)
Dilokpimol, A., Peng, M., Di Falco, M., Chin, A., Woeng, T., Hegi, R.M.W., Granchi, Z., Tsang, A., Hildén, K.S., Mäkelä, M.R., de Vries, R.P.: Penicillium subrubescens adapts its enzyme production to the composition of plant biomass. Bioresour. Technol. 311, 123477 (2020). https://doi.org/10.1016/j.biortech.2020.123477
Novy, V., Nielsen, F., Seiboth, B., Nidetzky, B.: The influence of feedstock characteristics on enzyme production in Trichoderma reesei: A review on productivity, gene regulation and secretion profiles. Biotechnol. Biofuels. 12, 1–16 (2019). https://doi.org/10.1186/s13068-019-1571-z
Dutta, T., Sahoo, R., Sengupta, R., Ray, S.S., Bhattacharjee, A., Ghosh, S.: Novel cellulases from an extremophilic filamentous fungi Penicillium citrinum: production and characterization. J. Ind. Microbiol. Biotechnol. 35, 275–282 (2008). https://doi.org/10.1007/s10295-008-0304-2
Gomes, A.F.S., dos Santos, B.S.L., Franciscon, E.G., Baffi, M.A.: Substract and temperature effect on xylanase production by Aspergillus fumigatus using low cost agricultural wastes. Biosci. J. 32(4), 915–921 (2016). https://doi.org/10.14393/bj-v32n4a2016-32935
Carrillo-Nieves, D., Saldarriaga-Hernandez, S., Gutiérrez-Soto, G., Rostro-Alanis, M., Hernández-Luna, C., Alvarez, A.J., Iqbal, H.M.N., Parra-Saldívar, R.: Biotransformation of agro-industrial waste to produce lignocellulolytic enzymes and bioethanol with a zero waste. Biomass Convers. Biorefinery. (2020). https://doi.org/10.1007/s13399-020-00738-6
Lopes, A.M., Oliveira-Nascimento, L. de, Ribeiro, A., Tairum, C.A., Breyer, C.A., Oliveira, M.A. de, Monteiro, G., Souza-Motta, C.M. de, Magalhães, P. de O., Avendaño, J.G.F., Cavaco-Paulo, A.M., Mazzola, P.G., Rangel-Yagui, C. de O., Sette, L.D., Converti, A., Pessoa, A.: Therapeutic l-asparaginase: upstream, downstream and beyond. Crit. Rev. Biotechnol. 37, 82–99 (2017). Doi: https://doi.org/10.3109/07388551.2015.1120705
Melicherová, K., Krahulec, J., Šafránek, M., Lišková, V., Hopková, D., Széliová, D., Turňa, J.: Optimization of the fermentation and downstream processes for human enterokinase production in Pichia pastoris. Appl. Microbiol. Biotechnol. 101, 1927–1934 (2017). https://doi.org/10.1007/s00253-016-7960-3
das Neves, C.A., de Menezes, L.H.S., Soares, G.A., dos Santos Reis, N., Tavares, I.M.C., Franco, M., de Oliveira, J.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
Infanzón-Rodríguez, M.I., Ragazzo-Sánchez, J.A., del Moral, S., Calderón-Santoyo, M., Aguilar-Uscanga, M.G.: Production and characterization of an enzyme extract with cellulase activity produced by an indigenous strain of Fusarium verticillioides ITV03 using sweet sorghum bagasse. Biotechnol. Lett. 42, 2271–2283 (2020). https://doi.org/10.1007/s10529-020-02940-y
Acknowledgments
The authors would like to thank the National Council of Science and Technology and Secretariat of Energy of Mexico for supporting this study through the Energy Sustainability Fund (FSE CONACYT-SENER). We thank our colleague Dr. Ángeles Calixto Romo from El Colegio de la Frontera Sur for the kindly donation of the fungus Penicillum citrinum CGETCR. We would also like to thank Montserrat del Socorro Valle Pérez for digital illustration of Fig. 6 and graphical abstract.
Funding
This study was funded by the Energy Sustainability Fund CONACYT-SENER [Project number 245750]. A.U. Valle-Pérez received a grant from the project 245750.
Author information
Authors and Affiliations
Contributions
Conceptualization, methodology, formal analysis and investigation, writing-original draft preparation, supervision: Lorena Amaya-Delgado and Alexander Uriel Valle-Pérez. Writing-review and editing: Lorena Amaya-Delgado, Guillermo Flores-Cosío and Alexander Uriel Valle-Pérez. Resources: Lorena Amaya-Delgado.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Valle-Pérez, A.U., Flores-Cosío, G. & Amaya-Delgado, L. Bioconversion of Agave Bagasse to Produce Cellulases and Xylanases by Penicillium citrinum and Aspergillus fumigatus in Solid-State Fermentation. Waste Biomass Valor 12, 5885–5897 (2021). https://doi.org/10.1007/s12649-021-01397-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12649-021-01397-y