Fungal Pretreatment of Corn Stover by Fomes sp. EUM1: Simultaneous Production of Readily Hydrolysable Biomass and Useful Biocatalysts

  • Jazmín Edith Méndez-Hernández
  • Octavio Loera
  • Edna Madai Méndez-Hernández
  • Esperanza Herrera
  • Oscar Arce-Cervantes
  • Nicolás Óscar Soto-Cruz
Original Paper

Abstract

Purpose

In this work we studied two approaches for the revalorization of corn stover (CS): Feedstock for bioethanol generation and substrate for the production of biocatalysts. The practical application of two of these biocatalysts (laccases and cellulases) was also evaluated.

Methods

The hydrolysis of CS was improved through a pretreatment with the thermotolerant fungus Fomes sp. EUM1; simultaneously, enzymatic extracts enriched with laccases or cellulases were obtained and applied for the pretreatment or hydrolysis of untreated CS.

Results

After 7 days, the fungal pretreatment promoted a significant increase in the release of reducing sugars (60%) and in the hydrolysis rate (50%). Lignin content decreased 61.2%, while holocellulose remained practically unchanged; a significant positive correlation (r = 0.948, p = 0.01) was found between laccase production and lignin degradation. Regarding biocatalysts application, the cellulases of Fomes sp. EUM1 showed catalytic properties similar to those of commercial enzymes; in addition, the pretreatment with laccases reduced 70% the processing-time (compared to the fungal treatment), and improved the release of reducing sugars and the hydrolysis rate by 26 and 29%, respectively.

Conclusion

The pretreatment of CS with Fomes sp. EUM1 produces two valuable products: saccharificable biomass useful for bioethanol production and highly active enzymes applicable in bioconversion processes.

Graphical Abstract

Keywords

Corn stover Biological pretreatments Bioethanol Enzymatic hydrolysis Lignocellulolytic enzymes White-rot fungi 

Notes

Acknowledgements

This work was funded by the Tecnológico Nacional de México (DGO-PYR-2015-072). Méndez-Hernández JE (Reg. No. 268164) thanks Mexican Nacional Council for Science and Technology (CONACyT) for the scholarship. The authors declare that they have no conflicts of interest.

References

  1. 1.
    BP Statistical Review of World Energy June 2017. (2017)Google Scholar
  2. 2.
    Sheehan, J., Aden, A., Paustian, K., Killian, K., Brenner, J., Walsh, M., Nelson, R.: Energy and environmental aspects of using corn stover for fuel ethanol. ‎J. Ind. Ecol. 7, 117–146 (2003)CrossRefGoogle Scholar
  3. 3.
    Renewable Fuel Association. Going Global: 2015 Ethanol Industry Outlook. Renewable Fuel Association, Washington, DC (2015)Google Scholar
  4. 4.
    Wheals, A.E., Basso, L.C., Alves, D.M., Amorim, H.V.: Fuel ethanol after 25 years. Trends Biotechnol. 17, 482–487 (1999)CrossRefGoogle Scholar
  5. 5.
    Wan, C., Li, Y.: Microbial pretreatment of corn stover with Ceriporiopsis subvermispora for enzymatic hydrolysis and ethanol production. Bioresour. Technol. 101, 6398–6403 (2010)CrossRefGoogle Scholar
  6. 6.
    USDA-NASS.: Agricultural statistics data base. National statistics for corn, https://www.nass.usda.gov/Statistics_by_Subject/index.php?sector=CROPS (2016). Accessed 29 Nov 2016
  7. 7.
    Instituto Nacional de Estadística y Geografía (INEGI): El sector alimentario en México 2014, Serie estadísticas sectoriales. Instituto Nacional de Estadística y Geografía (INEGI), México (2014)Google Scholar
  8. 8.
    Sun, F.H., Li, J., Yuan, Y.X., Yan, Z.Y., Liu, X.F.: Effect of biological pretreatment with Trametes hirsuta yj9 on enzymatic hydrolysis of corn stover. Int. Biodeterior. Biodegradation 65, 931–938 (2011)CrossRefGoogle Scholar
  9. 9.
    Perlack, R.D., Wright, L.L., Turhollow, A.F., Graham, R.L., Stokes, B.J., Erbach, D.C.: Biomass as feedstock for a bioenergy and bioproducts industry: the technical feasibility of a billion-ton annual supply. Department of Energy/GO-102005-2135. U.S. (2005)Google Scholar
  10. 10.
    Gao, Z., Mori, T., Kondo, R.: The pretreatment of corn stover with Gloeophyllum trabeum KU-41 for enzymatic hydrolysis. Biotechnol. Biofuels 5, 1–11 (2012)CrossRefGoogle Scholar
  11. 11.
    Öhgren, K., Bura, R., Saddler, J., Zacchi, G.: Effect of hemicellulose and lignin removal on enzymatic hydrolysis of steam pretreated corn stover. Bioresour. Technol. 98, 2503–2510 (2007)CrossRefGoogle Scholar
  12. 12.
    Torget, T., Walter, P., Himmel, M., Grohmann, K.: Dilute-acid pretreatment of corn residues and short-rotation woody crops. Appl. Biochem. Biotechnol. 28, 75–86 (1991)CrossRefGoogle Scholar
  13. 13.
    da Costa Sousa, L., Chundawat, S.P., Balan, V., Dale, B.E.: ‘Cradle-to-grave’ assessment of existing lignocellulose pretreatment technologies. Curr. Opin. Biotechnol. 20, 339–347 (2009)CrossRefGoogle Scholar
  14. 14.
    Wang, F.Q., Xie, H., Chen, W., Wang, E.T., Du, F.G., Song, A.D.: Biological pretreatment of corn stover with ligninolytic enzyme for high efficient enzymatic hydrolysis. Bioresour. Technol. 144, 572–578 (2013)CrossRefGoogle Scholar
  15. 15.
    Mohanram, S., Rajan, K., Carrier, D.J., Nain, L., Arora, A.: Insights into biological delignification of rice stuntreated by Trametes hirsuta and Myrothecium roridum and comparison of hydrolysis yields with dilute acid pretreatment. Biomass. Bioenergy. 76, 54–60 (2015)CrossRefGoogle Scholar
  16. 16.
    Van Soest, P.V., Robertson, J.B., Lewis, B.A.: Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74, 3583–3597 (1991)CrossRefGoogle Scholar
  17. 17.
    Wolfenden, B.S., Willson, R.L.: Radical-cations as reference chromogens in kinetic studies of ono-electron transfer reactions: pulse radiolysis studies of 2,2′-azinobis-(3-ethylbenzthiazoline-6-sulphonate)., J. Chem. Soc. Perkin Trans. 2. 0, 805–812 (1982)Google Scholar
  18. 18.
    Archibald, F.S.: A new assay for lignin-type peroxidases employing the dye azure B. Appl. Environ. Microbiol. 58, 3110–3116 (1992)Google Scholar
  19. 19.
    Kuwahara, M., Glenn, J.K., Morgan, M.A., Gold, M.H.: Separation and characterization of two extracelluar H2O2-dependent oxidases from ligninolytic cultures of Phanerochaete chrysosporium. FEBS Lett. 169, 247–250 (1984)CrossRefGoogle Scholar
  20. 20.
    Shin, K., Oh, I., Kim, C.: Production and purification of Remazol Brilliant Blue R decolorizing peroxidase from the culture filtrate of Pleurotus ostreatus. Appl. Environ. Microbiol. 63, 1744–1748 (1997)Google Scholar
  21. 21.
    Ghose, T.K.: Measurement of cellulase activities. Pure Appl. Chem. 59, 257–268 (1987)CrossRefGoogle Scholar
  22. 22.
    Loera, O., Córdova, J.: Improvement of xylanase production by a parasexual cross between Aspergillus niger strains. Braz. Arch. Biol. Technol. 46, 177–181 (2003)CrossRefGoogle Scholar
  23. 23.
    Arce-Cervantes, O., Mendoza, G., Miranda, L., Meneses, M., Loera, O.: Efficiency of lignocellulolytic extracts from thermotolerant strain Fomes sp. EUM1: stability and digestibility of agricultural wastes. J. Agric. Sci. Technol. 15, 229–240 (2013)Google Scholar
  24. 24.
    Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976)CrossRefGoogle Scholar
  25. 25.
    Miller, G.L.: Use of dinitrosalicylic acid reagent for determination of reducing sugar. ‎Anal. Chem. 31, 426–428 (1959)Google Scholar
  26. 26.
    McMillan, J.D.: Pretreatment of lignocellulosic biomass. In: Himmel, M.E., Baker, J.O., Overend, R.P. (eds.) Enzymatic Conversion of Biomass for Fuels Production, pp. 292–324. American Chemical Society, Washington, DC (1994)CrossRefGoogle Scholar
  27. 27.
    Yu, H., Du, W., Zhang, J., Ma, F., Zhang, X., Zhong, W.: Fungal treatment of corn stover enhances the delignification and xylan loss during mild alkaline pretreatment and enzymatic digestibility of glucan. Bioresour. Technol. 101, 6728–6734 (2010)CrossRefGoogle Scholar
  28. 28.
    Zhao, L., Cao, G.L., Wang, A.J., Ren, H.Y., Dong, D., Liu, Z.N., Guan, X.Y., Xu, C.J., Ren, N.Q.: Fungal pretreatment of corn stover with Phanerochaete chrysosporium for enhancing enzymatic hydrolysis and hydrogen production. Bioresour. Technol. 114, 365–369 (2012)CrossRefGoogle Scholar
  29. 29.
    Saha, B.C., Qureshi, N., Kennedy, G.J., Cotta, M.A.: Biological pretreatment of corn stover with white-rot fungus for improved enzymatic hydrolysis. Int. Biodeterior. Biodegradation 109, 29–35 (2016)CrossRefGoogle Scholar
  30. 30.
    Chen, F., Dixon, R.A.: Lignin modification improves fermentable sugar yields for biofuel production. Nat. Biotechnol. 25, 759–761 (2007)CrossRefGoogle Scholar
  31. 31.
    Müller, H.W., Trösch, W.: Screening of white-rot fungi for biological pretreatment of wheat stuntreated for biogas production. Appl. Microbiol. Biotechnol. 24, 180–185 (1986)CrossRefGoogle Scholar
  32. 32.
    Cianchetta, S., Di Maggio, B., Burzi, P.L., Galletti, S.: Evaluation of selected white-rot fungal isolates for improving the sugar yield from wheat stuntreated. Appl. Biochem. Biotechnol. 173, 609–623 (2014)Google Scholar
  33. 33.
    Sánchez, C.: Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol. Adv. 27, 185–194 (2009)CrossRefGoogle Scholar
  34. 34.
    García-Torreiro, M., López-Abelairas, M., Lu-Chau, T.A., Lema, J.M.: Fungal pretreatment of agricultural residues for bioethanol production. Ind. Crops Prod. 89, 486–492 (2016)CrossRefGoogle Scholar
  35. 35.
    Ordaz-Hernández, A., Ortega-Sánchez, E., Montesinos-Matías, R., Hernández-Martínez, R., Torres-Martínez, D., Loera, O.: Morphological and enzymatic response of the thermotolerant fungus Fomes sp. EUM1 in solid state fermentation under thermal stress. FEMS Microbiol. Lett. 363, 1–6 (2016)CrossRefGoogle Scholar
  36. 36.
    Ordaz, A., Favela, E., Meneses, M., Mendoza, G., Loera, O.: Hyphal morphology modification in thermal adaptation by the white-rot fungus Fomes sp. EUM1. J. Basic Microbiol. 52, 167–174 (2012)CrossRefGoogle Scholar
  37. 37.
    Membrillo, I., Sánchez, C., Meneses, M., Favela, E., Loera, O.: Particle geometry affects differentially substrate composition and enzyme profiles by Pleurotus ostreatus growing on sugar cane bagasse. Bioresour. Technol. 102, 1581–1586 (2011)CrossRefGoogle Scholar
  38. 38.
    Kadimaliev, D.A., Revin, V.V., Atykyan, N.A., Samuilov, V.D.: Effect of wood modification on lignin consumption and synthesis of lignolytic enzymes by the fungus Panus (Lentinus) tigrinus. Appl. Biochem. Microbiol. 39, 488–492 (2003)CrossRefGoogle Scholar
  39. 39.
    Saqib, A.A.N., Whitney, P.J.: Role of fragmentation activity in cellulose hydrolysis. Int. Biodeterior. Biodegrad. 58, 180–185 (2006)CrossRefGoogle Scholar
  40. 40.
    Morgavi, D.P., Beauchemin, K.A., Nsereko, V.L., Rode, L.M., McAllister, T.A., Wang, Y.: Trichoderma enzymes promote Fibrobacter succinogenes S85 adhesion to, and degradation of, complex substrates but not pure cellulose. ‎J. Sci. Food Agric. 84, 1083–1090 (2004)CrossRefGoogle Scholar
  41. 41.
    Qiu, W., Chen, H.: Enhanced the enzymatic hydrolysis efficiency of wheat stuntreated after combined steam explosion and laccase pretreatment. Bioresour. Technol. 118, 8–12 (2012)CrossRefGoogle Scholar
  42. 42.
    Moreno, A.D., Ibarra, D., Fernández, J.L., Ballesteros, M.: Different laccase detoxification strategies for ethanol production from lignocellulosic biomass by the thermotolerant yeast Kluyveromyces marxianus CECT 10875. Bioresour. Technol. 106, 101–109 (2012)CrossRefGoogle Scholar
  43. 43.
    Moilanen, U., Kellock, M., Galkin, S., Viikari, L.: The laccase-catalyzed modification of lignin for enzymatic hydrolysis. Enzyme Microb. Technol. 49, 492–498 (2011)CrossRefGoogle Scholar
  44. 44.
    Palonen, H., Viikari, L.: Role of oxidative enzymatic treatments on enzymatic hydrolysis of softwood. ‎Biotechnol. Bioeng. 86, 550–557 (2004)CrossRefGoogle Scholar
  45. 45.
    Gutiérrez, A., Rencoret, J., Cadena, E.M., Rico, A., Barth, D., José, C., Martínez, A.T.: Demonstration of laccase-based removal of lignin from wood and non-wood plant feedstocks. Bioresour. Technol. 119, 114–122 (2012)CrossRefGoogle Scholar
  46. 46.
    Chen, Q., Marshall, M.N., Geib, S.M., Tien, M., Richard, T.L.: Effects of laccase on lignin depolymerization and enzymatic hydrolysis of ensiled corn stover. Bioresour. Technol. 117, 186–192 (2012)CrossRefGoogle Scholar
  47. 47.
    Chen, M., Zhao, J., Xia, L.: Comparison of four different chemical pretreatments of corn stover for enhancing enzymatic digestibility. Biomass Bioenergy. 33, 1381–1385 (2009)CrossRefGoogle Scholar
  48. 48.
    Wan, C., Li, Y.: Microbial delignification of corn stover by Ceriporiopsis subvermispora for improving cellulose digestibility. Enzyme Microb. Technol. 47, 31–36 (2010)CrossRefGoogle Scholar
  49. 49.
    Kim, S., Holtzapple, M.T.: Lime pretreatment and enzymatic hydrolysis of corn stover. Bioresour. Technol. 96, 1994–2006 (2005)CrossRefGoogle Scholar
  50. 50.
    Torget, R., Walter, P., Himmel, M., Grohmann, K.: Dilute-acid pretreatment of corn residues and short-rotation woody crops. Appl. Biochem. Biotechnol. 28, 75–86 (1991)CrossRefGoogle Scholar
  51. 51.
    Shi, J., Sharma-Shivappa, R.R., Chinn, M., Howell, N.: Effect of microbial pretreatment on enzymatic hydrolysis and fermentation of cotton stalks for ethanol production. Biomass Bioenergy. 33, 88–96 (2009)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Chemical and Biochemical EngineeringInstituto Tecnológico de DurangoDurangoMexico
  2. 2.Department of BiotechnologyUniversidad Autónoma Metropolitana IztapalapaMexico CityMexico
  3. 3.Institute of Scientific ResearchUniversidad Juárez del Estado de DurangoDurangoMexico
  4. 4.Faculty of Veterinary Medicine and ZootechnyUniversidad Juárez del Estado de DurangoDurangoMexico
  5. 5.Institute of Agricultural SciencesUniversidad Autónoma del Estado de HidalgoHidalgoMexico

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