Abstract
Lignocellulose in maize straw includes cellulose, hemicellulose, and lignin, and the degradation of lignocellulose is a complex process in which multiple enzymes are jointly involved. In exploring the co-degradation of a certain substrate by multiple enzymes, different enzymes are combined freely for the achievement of the effective synergism. Additionally, some organic acids and small molecule aromatic compounds can also increase the enzymatic activity of lignin enzymes and improve the degradation rate of lignin. In this study, manganese peroxidase (MnP) from Irpex lacteus (I. lacteus) was heterologously expressed in food-grade Schizosaccharomyces pombe (S. pombe). The multiple enzymes co-fermentation conditions were initially screened by orthogonal tests: 0.5% CaCl2, 1% 10,000 U/g Laccase (Lac), 0.3% MnSO4, and 0.4% glucose oxidase (GOD). It was showed that the lignin degradation rate could reach 65.85% after 3 days of synergistic degradation with the addition of 0.02% Tween-80, 0.5 mM oxalic acid. This indicates that oxalic acid has a promoting effect on the activity of MnP, and the promoting effect is more significant when Tween-80 is complexed with oxalic acid.
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References
Kun, L., Hongwu, W., Xiaojiao, H., Zhifang, L., Yujin, W., Changling, H., & Zabotina, O. A. (2016). Genome-wide association study reveals the genetic basis of stalk cell wall components in maize. PLoS One, 11(8), e0158906.
Huang, S., Wu, Q., Zhou, D., Huang, R. (2015) Thermal decomposition properties of materials from different parts of corn stalk. BioResources, 10(2), 2020–2031. https://doi.org/10.15376/biores.10.2.2020-2031
Katongole, C. B., BakEeVa, A., Passoth, V., & Lindberg, J. E. (2017). Effect of solid-state fermentation with Arxula adeninivorans or Hypocrea jecorina (anamorph Trichoderma reesei) on hygienic quality and in-vitro digestibility of banana peels by mono-gastric animals. Livestock Science, 199, 14–21.
Li, Y., Yu, C., Zhu, W., & Tao, S. (2012). Effect of complex lactic acid bacteria on silage quality and in vitro dry matter digestibility of corn straw. Journal of Animal and Veterinary Advances, 11(9), 1395–1399.
Yuan, H. A., Jd, A., Asms, B., Tmbm, C., Mak, C., Whh, A., & Jwc, A. (2019). The nutritional value of the lower maize stem cannot be improved by ensiling nor by a fungal treatment – Science direct. Animal Feed Science and Technology, 247, 92–102.
Zeng, Y., Zhao, S., Yang, S., & Ding, S. Y. (2014). Lignin plays a negative role in the biochemical process for producing lignocellulosic biofuels. Current Opinion in Biotechnology, 27, 38–45.
Jin, Y., Na, Y., Tong, Q., Jin, Z., & Xu, X. (2016). Intensification of sodium hydroxide pretreatment of corn stalk using magnetic field in a fluidic system. Bioresource Technology, 220, 1–7.
Akpinar, M., & Ozturk, U. R. (2020). Decolorization and degradation potential of enhanced lignocellulolytic enzymes production by Pleurotus eryngii using cherry waste from industry. Biotechnology & Applied Biochemistry, 67(5), 760–773. https://doi.org/10.1002/bab.1846
Li, K., Wang, H., Hu, X., Liu, Z., Wu, Y., Huang, C., & Zabotina, O. A. (2016). Genome-wide association study reveals the genetic basis of stalk cell wall components in maize. PLoS One, 11, e0158906.
Huang, S., Wu, Q., Zhou, D., & Huang, R. (2015). Thermal decomposition properties of materials from different parts of corn stalk. BioResources, 10, 2020.
Awawdeh, M. S. (2011). Alternative feedstuffs and their effects on performance of Awassi sheep: A review. Tropical Animal Health and Production, 43, 1297–1309. https://doi.org/10.1007/s11250-011-9851-z
Xing, Q., Su, X., Luo, H., Rui, M., & Ma, F. (2018). Deciphering lignocellulose deconstruction by the white rot fungus Irpex lacteus based on genomic and transcriptomic analyses. Biotechnology for Biofuels, 11, 58.
Zhang, S., Xiao, J., Wang, G., & Chen, G. (2020). Enzymatic hydrolysis of lignin by ligninolytic enzymes and analysis of the hydrolyzed lignin products. Bioresource Technology, 304, 122975.
Merino, C., Kuzyakov, Y., Godoy, K., Cornejo, P., & Matus, F. (2020). Synergy effect of peroxidase enzymes and Fenton reactions greatly increase the anaerobic oxidation of soil organic matter. Scientific Reports, 10(1), 1–12. https://doi.org/10.1038/s41598-020-67953-z
Wang, F., Huang, F., & Ai, M. (2019). Synergetic depolymerization of aspen CEL by pyranose 2-oxidase and lignin-degrading peroxidases. BioResources, 14, 3481–3494.
Wu, K., Yan, S., Lu, H., Li, H., & Wang, Q. (2016). Difference in the activity of extracellular Lignocellulolytic enzymes and the intracellular proteome of induced by different wood substrates. Scientia Silvae Sinicae, 52(8), 157–166. https://doi.org/10.11707/j.1001-7488.20160819
Zhou-lei, C. U. I., Hong-cheng, W. A. N. G., Jun-ming, W. U., & Hua-you, C. H. E. N. (2020). Expression and enzymatic properties of a manganese peroxidase from Irpex Iacteus. Journal of Biology, 37(06), 46–50.
Mao, Y., Luo, B., & Hou, G. (2015). Uncertainly evaluation of determination of crude fiber in cottonsced meal by filter bag method[J]. China Feed. https://doi.org/10.15906/j.cnki.cn11-2975/s.20151808
Rekik, H., Zaraî Jaouadi, N., Bouacem, K., et al. (2019). Physical and enzymatic properties of a new manganese peroxidase from the white-rot fungus Trametes pubescens strain i8 for lignin biodegradation and textile-dyes biodecolorization. International Journal of Biological Macromolecules, 125, 514–525. https://doi.org/10.1016/j.ijbiomac.2018.12.053
Crestini, C., Crucianelli, M., Orlandi, M., & Saladino, R. (2010). Oxidative strategies in lignin chemistry: A new environmental friendly approach for the functionalisation of lignin and lignocellulosic fibers. Catalysis Today, 156, 8–22.
Fan, J., Lou, L., Zhang, L., et al. (2019). The effect of glucose oxidase, gluconic acid and honey-sosurced additives on growth performance and nutrient digestibility of Yellow broilers[J]. Animal Husbandry & Veterinary Medicine, 51(10), 26–30.
Tang, H., Gao, X., Yao, B., et al. (2015). Study on the bacteriostatic and acid producing effect of glucose oxidase in vitro[J]. Feed Industry, 36(10), 13–16. https://doi.org/10.13302/j.cnki.fi.2015.10.004
Gong, Y., Zhang, C., Yan, Q., et al. (2015). Enhanced enzymatic hydrolysis of sugarcane bagasse hemicellulose using recombinant glucose oxidase expressed by Pichia pastoris. Industrial Crops & Products, 77, 458–466. https://doi.org/10.1016/j.indcrop.2015.07.038
Glenn, J. K., & Gold, M. H. (1985). Purification and characterization of an extracellular Mn(II)-dependent peroxidase from the lignin-degrading basidiomycete, Phanerochaete chrysosporium. Archives of Biochemistry & Biophysics, 242, 329–341.
Bermek, H., Li, K., & Eriksson, K. (2002). Studies on mediators of manganese peroxidase for bleaching of wood pulps. Bioresource Technology, 85, 249–252.
Alfi, A., Z§, Bo., Damnjanovi, J., et al. (2019). Production of active manganese peroxidase in Escherichia coli by co-expression of chaperones and invitro maturation by ATP-dependent chaperone release [J]. Journal of Bioscience and Bioengineering, 128(3), 290–295.
Ram, A., & F, J. (2014). The cell wall stress response in Aspergillus niger involves increased expression of the glutamine : Fructose-6-phosphate amidotransferase-encoding gene (gfaA) and increased deposition of chitin in the cell wall. Microbiology, 150(10), 3315–26.
Morsi, R., Bilal, M., Iqbal, H. M. N., & Ashraf, S. S. (2020). Laccases and peroxidases: The smart, greener and futuristic biocatalytic tools to mitigate recalcitrant emerging pollutants. Science of The Total Environment, 714, 136572.
Mei, Y. U., Xiao-Wen, R., Tan, L. Q., et al. (2014). Study on impact factors of manganese-dependent peroxidase produced by white rot fungi[J]. Chemistry & Bioengineering, 11, 40–44. https://doi.org/10.3969/j.issn.0438-1157.2014.12.10
Asther, M., Lesage, L., Drapron, R., Corrieu, G., & Odier, E. (1988). Phospholipid and fatty acid enrichment of Phanerochaete chrysosporium INA-12 in relation to ligninase production. Applied Microbiology & Biotechnology, 27, 393–398.
Bao, W., Fukushima, Y., Jensen, K. A., Jr., Moen, M. A., & Hammel, K. E. (1994). Oxidative degradation of non-phenolic lignin during lipid peroxidation by fungal manganese peroxidase. FEBS Lett, 354(3), 297–300. https://doi.org/10.1016/0014-5793(94)01146-x
Wariishi, H., Valli, K., Renganathan, V., & Gold, M. H. (1989). Thiol-mediated oxidation of nonphenolic lignin model compounds by manganese peroxidase of Phanerochaete chrysosporium. Journal of Biological Chemistry, 264, 14185–14191.
Picart, P., Sevenich, M., María, P., & Schallmey, A. (2015). Exploring glutathione lyases as biocatalysts: Paving the way for enzymatic lignin depolymerization and future stereoselective applications. Green Chemistry, 17, 4931.
Mori, T., Ikeda, K., Kawagishi, H., & Hirai, H. (2021). Improvement of saccharide yield from wood by simultaneous enzymatic delignification and saccharification using a ligninolytic enzyme and cellulase. Journal of Bioscience and Bioengineering, 132(3), 213–219. https://doi.org/10.1016/j.jbiosc.2021.04.016
Barbosa, A. M., Dekker, R., & Hardy, G. (2010). Veratryl alcohol as an inducer of laccase by an ascomycete, Botryosphaeria sp., when screened on the polymeric dye Poly R-478. Letters in Applied Microbiology, 23, 93–96.
Niladevi, K. N., & Prema, P. (2008). Effect of inducers and process parameters on laccase production by Streptomyces psammoticus and its application in dye decolourization. Bioresource Technology, 99, 4583–4589.
Naveed, M., Muhammad, A., Tahir, I. M., et al. (2015). Utilization of agro-wastes for production of ligninolytic enzymes in liquid state fermentation by Phanerochaete chrysosporium-Ibl-03[J]. International Journal of Chemical and Biochemical Sciences, 7, 9–14.
Selvaraj, B., Sanjeevirayar, A., & Rajendran, A. (2015). Laccase production using mixed substrates containing lignocellulosic materials by Pleurotus ostreatus in submerged liquid culture. International Journal of ChemTech Research, 7, 355–368.
Elisashvili, V., & Kachlishvili, E. (2009). Physiological regulation of laccase and manganese peroxidase production by white-rot Basidiomycetes. Journal of Biotechnology, 144, 37–42.
Xing, Q., Su, X., Luo, H., et al. (2018). Deciphering lignocellulose deconstruction by the white rot fungus Irpex lacteus based on genomic and transcriptomic analyses. Biotechnology for Biofuels, 11(1), 58.
Funding
This study was financially supported by the national key research and development program (2021YFC2103004, 2021YFA0910402), by the Open Funding Project of the State Key Laboratory of Biochemical Engineering, China (2018KF-02), and by Key Research and Development Program (Social Development) of Zhenjiang City (SH2020021).
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Chen, H., Li, S., Cui, Z. et al. Synergistic Degradation of Maize Straw Lignin by Manganese Peroxidase from Irpex lacteus. Appl Biochem Biotechnol 195, 3855–3871 (2023). https://doi.org/10.1007/s12010-022-04189-9
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DOI: https://doi.org/10.1007/s12010-022-04189-9