Abstract
Treatment of plant biomass with ozone is a promising delignification method. It was shown that lignin removal from the cell wall during ozonation was limited by topochemical reactions and toke place in the secondary rather in the primary cell wall. The separation of cellulose microfibrils, the loss of cell wall stiffness and complete removal of intercellular substance during the delignification process were visualized by SEM. The dependence of the average diameter of the cellulose microfibril aggregates in the cell wall of ozonized straw on ozone consumption was studied. Lignin removal caused an increase of size of cellulose microfibrils aggregates. It was demonstrated that there was an optimal degree of delignification, at which cellulose became more accessible to enzymes in the subsequent bioconversion processes. The data on the ozone consumption, residual lignin content, and sugars yield in the enzymatic hydrolysis of ozonized wheat straw were obtained. It was also found that the optimum delignification degree for sugars yield was ≈10% of residual lignin content and optimum ozone consumption was 2 mol·О3/mol C9PPU (phenylpropane structural unit) of lignin in raw straw.
Funding source: The Russian Federation Ministry of Education and Science
Funding source: M.V. Lomonosov Moscow State University Program of Development
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: The research was supported by the Russian Federation Ministry of Education and Science and by M.V. Lomonosov Moscow State University Program of Development. The equipment of Center for Collective Use of Scientific Equipment “Arctic” (Northern Arctic) Federal University, Russian Federation was used in this research.
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Aldaeus, F. and Sjöholm, E. (2011). COST Action FP0901 Round Robins of lignin samples Part 1: Lignin content. Version 3 (2010-12-14). Innventia Report No.: IR 108. fredrik.aldaeus@innventia.com.Search in Google Scholar
Bailey, P. S. (1982). Ozonation in organic chemistry, Vol II. Acad Press, New York, NY.Search in Google Scholar
Ben’ko, E.M., Manisova, O.R., and Lunin, V.V. (2017a). Effect of moisture content on the interaction between lignocellulosic materials and ozone. Russ. J. Phys. Chem. A 91: 1117–1123. https://doi.org/10.1134/S0036024417070056.Search in Google Scholar
Ben’ko, E.M., Chukhchin, D.G., and Lunin, V.V. (2017b). Ozone pretreatment and fermentative hydrolysis of wheat straw. Russ. J. Phys. Chem. A 91: 2092–2097. https://doi.org/10.1134/S0036024417110036.Search in Google Scholar
Ben’ko, E.M., Chukhchin, D.G., Mamleeva, N.A., Kharlanov, A.N., and Lunin, V.V. (2020). Ozonolytic delignification of wheat straw. Russ. J. Phys. Chem. A 94: 1535–1542. https://doi.org/10.1134/S0036024420080038.Search in Google Scholar
Bertaud, F., Croué, J.P., and Legube, B. (2001). Ozonation of β-O-4 Dimer Lignin Model: By-Products Identification and Reaction Pathways. Ozone Sci. Eng. 23, 139–148. https://doi.org/10.1080/01919510108961996.Search in Google Scholar
Binder, A., Pelloni, L., and Fiechter, A. (1980). Delignification of straw with ozone to enhance biodegradability. Eur. J. Appl. Microbiol. Biotechnol. 11: 1–5.10.1007/BF00514070Search in Google Scholar
Bonnet, M. and Dore, M. (1989). Identification of ozonation by-products of lignin and carbohydrates in water. Environ. Technol. Lett. I 10: 577–590.10.1080/09593338909384775Search in Google Scholar
Bule, M.V., Gao, A.H., Hiscox, B., and Chen, S. (2013). Structural modification of lignin and characterization of pretreated wheat straw by ozonation. J. Agri. Food Chem. 61: 3916–3925. https://doi.org/10.1021/jf4001988.Search in Google Scholar PubMed
Chang, V.S. and Holtzapple, M.T. (2000). Fundamental factors affecting biomass enzymatic reactivity. Appl. Biochem. Biotechnol. 84: 5–37. https://doi.org/10.1385/ABAB:84-86:1-9:5.10.1007/978-1-4612-1392-5_1Search in Google Scholar
Crestini, C. and Argyropoulos, D.S. (1997). Structural аnalysis of wheat straw lignin by quantitative 31P and 2D NMR spectroscopy. The occurrence of ester bonds and α-O-4 substructures. J. Agri. Food Chem. 45: 1212–1219.10.1021/jf960568kSearch in Google Scholar
De Barros, R.D.R.O., Paredes, R.D.S., Endo, T., Bon, E.P.D.S., and Lee, S.H. (2013). Association of wet disk milling and ozonolysis as pretreatment for enzymatic saccharification of sugarcane bagasse and straw. Biores. Technol. 136: 88–294. https://doi.org/10.1016/j.biortech.2013.03.009.Search in Google Scholar PubMed
Ding, D., Zhou, X., You, T., Zhang, X., Zhang, X., and slu, F. (2018). Exploring the mechanism of high degree of delignification inhibits cellulose conversion efficiency. Carbohydr. Polym. 181: 931–938. https://doi.org/10.1016/j.carbpol.2017.11.057.Search in Google Scholar
Dowe, N., and McMillan, J. (2001). SSF experimental protocols — lignocellulosic biomass hydrolysis and fermentation. Laboratory Analytical Procedure (LAP) Issue Date: 10/30/2001. National Renewable Energy Laboratory US, Indiana State Library, Indianapolis.Search in Google Scholar
Eriksson, O., Goring, D., and Lindgren, B. (1980). Structural studies on the chemical bonds between lignins and carbohydrates in spruce wood. Wood Sci. Technol. 4: 267–79. Holzforschung München, Technische Universität München, München, Germany.10.1007/BF00383454Search in Google Scholar
Ferron, B., Croué, J.P., Dore, M., 1995. Comparative study of ozonation of two lignin model compounds :coniferyl alcohol and ferulic acid. Identification of some by-Products. Ozone: Science. Engineering. 17, 687–699.10.1080/01919512.1995.10555779Search in Google Scholar
García-Cubero, M.T., Palacín, L.G., González-Benito, G., Bolado, S., Lucas, S., and Coca, M. (2012). An analysis of lignin removal in a fixed bed reactor by reaction of cereal straws with ozone. Biores. Technol. 107: 229–234. https://doi.org/10.1016/j.biortech.2011.12.010.Search in Google Scholar
Giummarella, N., Gunnar Henriksson, G., Salmén, L., and Lawoko, M. (2017). On the effect of hemicellulose removal on celluloselignin interactions. Nord. Pulp Pap. Res. J. 32: 542–549. https://doi.org/10.3183/NPPRJ-2017-32-04-p542-549.Search in Google Scholar
Hoigné, J. and Bader, H. (1983). Rate constants of reactions of ozone with organic and inorganic compounds in water-II. Water Res. 17:185–194. https://doi.org/10.1016/0043-1354(83)90099-4.Search in Google Scholar
Ji, Z., Ma, J., and Xu, F. (2014). Multiple-scale visualization of cell walls during alkali pretreatment. Micros. Microanal. 20: 566–576. https://doi.org/10.1017/S1431927614000063.Search in Google Scholar PubMed
Jin, Z., Katsumata, K.S., Lam, T.B.T., and Iiyama, K. (2006). Covalent linkages between cellulose and lignin in cell walls of coniferous and nonconiferous woods. Biopolymers 83: 103–110. https://doi.org/10.1002/bip.20533.Search in Google Scholar PubMed
Kádár, Z., Schultz-Jensen, N., Jensen, J.S., Hansen, M.A.T., Leipold, F., and Bjerre, A.B., (2015). Enhanced ethanol production by removal of cutin and epicuticular waxes of wheat straw by plasma assisted pretreatment. Biomass Bioenergy 81: 26–30. https://doi.org/10.1016/j.biombioe.2015.05.012.Search in Google Scholar
Kobayashi, M., Asano, T., Kajiyama, M., and Tomita, B. (2005). Effect of ozone treatment of wood on its liquefaction. J. Wood Sci. 51: 348–356. https://doi.org/10.1007/s10086-004-0664-9.Search in Google Scholar
Lam, T.B.T. and Iiyama, K. (2000). Characteristics of senescent straw cell walls of dwarf, semidwarf, and normal strains of rice (Oryza sativa) plants. J. Wood Sci. 46: 376–380. Received July, 9, 1999/Accepted Ocober, 1, 1999.10.1007/BF00776399Search in Google Scholar
Lawoko, M., Berggren, R., Berthold, F., Henriksson, G., and Gellerstedt, G. (2004). Changes in the lignin carbohydrate complex of softwood during kraft and oxygen delignification: Lignin-polysaccharide networks II. Holzforschung 58: 603–610. https://doi.org/10.1515/HF.2004.114.Search in Google Scholar
Lemeune, S., Barbe, J.M., Trichet, A., and Guilar, R. (2000). Degradation of cellulose models during an ozone treatment. Ozonation of glucose and cellobiose with oxygen or nitrogen as carrier gas at different pH. Ozone Sci. Eng. Iss. 5: 447–460. https://doi.org/10.1080/01919510009408789.Search in Google Scholar
Mamleeva, N.A., Autlov, S.A., Bazarnova, N.G., and Lunin, V.V., (2016). Degradation of polysaccharides and lignin in wood ozonation. Russ. J. Bioorgan. Chem. 42: 694–699. https://doi.org/10.1134/S1068162016070098.Search in Google Scholar
Marcq, O. and Barbe, J.M. (2009). Reaction pathways of glucose oxidation by ozone under acidic conditions. Carbohydr. Res. 344: 1303–1310. https://doi.org/10.1016/j.carres.2009.05.012.Search in Google Scholar PubMed
Matonina, N.A. (2015). Effect of low-enthalpy electron-beam plasma on wood and its components. Thesis for the degree in Chemical Sciences Northern (Arctic). Federal University, Publishing House V.N. Bulatova NArFU Arkhangel’sk, 20 p. https://narfu.ru/upload/iblock/d58/matonina_avtoreferat.pdf.Search in Google Scholar
Matonina, N.A., Chukhchin, D.G., and Sokolov, O.M., (2010). Destruction of pulp under influence of electron-beam plasma.ISSN 0536 - 1036. IVUZ For. J. 4: 74–83. https://cyberleninka.ru/article/n/destruktsiya-tsellyulozy-pod-deystviem-elektronno-puchkovoy-plazmy-epp/viewer.Search in Google Scholar
Nompex, P. and Dore, M. (1991). Ozonation of selected molecules constituting cellular metter. Ozone Sci. Eng. 13: 265–286. https://doi.org/10.1080/01919519108552467.Search in Google Scholar
Pan, G.Y., Chen, C.L., Gratzl, J.S., and Chang, H.M. (1995). Model compound studies on the cleavage of glycosidic bonds by ozone in aqueous solution. Res. Chem. Intermediat. 21: 205–222.10.1007/BF03052254Search in Google Scholar
Pönni, R., Galvis, L., and Vuorinen, T. (2014). Changes in accessibility of cellulose during kraft pulping of wood in deuterium oxide. Carbohydr. Pol. 101: 792–797. https://doi.org/10.1016/j.carbpol.2013.10.001.Search in Google Scholar PubMed
Ragnar, M., Eriksson, T., and Reitberger, T. (1999). Radical formation in ozone reactions with lignin and carbohydrate model compounds. Holzforschung 53: 423–428.10.1515/HF.1999.049Search in Google Scholar
Salmén, L. and Olsson, A.M. (1998). Interactions between hemicelluloses, lignin and cellulose: structure–property relationships. J. Pulp Pap. Sci. 24: 99–103.Search in Google Scholar
Sarkanen, K.V., Islam, A., and Anderson, C. (1992). Methods in lignin chemistry. Springer-Verlag, Berlin, pp. 387–406.10.1007/978-3-642-74065-7_26Search in Google Scholar
Sjöström, E. (1981). Wood Chemistry: fundamentals and applications. Academic Press Inc. ISBN: 012647480X,9780126474800, 223 p.Search in Google Scholar
Somogyi, M. (1952). Estimation of sugars by colorimetric method. J. Biol. Chem. 200: 245.Search in Google Scholar
Sugimoto, T., Magara, K., Hosoya, S., Oosawa, S., Shimoda, T., and Nishibori, K. (2009). Ozone pretreatment of lignocellulosic materials for ethanol production: improvement of enzymatic susceptibility of softwood. Holzforschung 63: 537–543. https://doi.org/10.1515/HF.2009.091.Search in Google Scholar
Tarasov, D., Leitch, M., and Fatehi, P. (2018). Lignin–carbohydrate complexes: properties, applications, analyses, and methods of extraction: a review. Biotechnol. Biofuel. 11: 269. https://doi.org/10.1186/s13068-018-1262-1.Search in Google Scholar PubMed PubMed Central
Travaini, R., Otero, M.D.M., Coca, M., Da-Silva, R., and Bolado, S. (2013). Sugarcane bagasse ozonolysis pretreatment: effect on enzymatic digestibility and inhibitory compound formation. Biores. Technol. 133: 332–339. https://doi.org/10.1016/j.biortech.2013.01.133.Search in Google Scholar PubMed
Travaini, R., Martín-Juárez, J., Lorenzo-Hernando, A., and Bolado-Rodríguez, S. (2016). Ozonolysis: an advantageous pretreatment for lignocellulosic biomass revisited. Biores. Technol. 199: 2–12. https://doi.org/10.1016/j.biortech.2015.08.143.Search in Google Scholar PubMed
Uma Maheswari, C., Obi Reddy, K., and Muzenda, E. (2014). Extraction, chemical composition, morphology and characterization of cellulose microfibrils from Ficus Leaves. J. Biobas. Mater. Bioener. 8: 409–414.10.1166/jbmb.2014.1452Search in Google Scholar
Wan, J., Wang, Y., and Xiao, Q. (2010). Effects of hemicellulose removal on cellulose fiber structure and recycling characteristics of eucalyptus pulp. Biores. Technol. 101: 4577–4583. https://doi.org/10.1016/j.biortech.2010.01.026.Search in Google Scholar PubMed
Wong, K.K.Y., Deverell, K.F., Mackie, K.L., Clark, T.A., and Donaldson, L.A. (1988). The relationship between fiber porosity and cellulose digestibility in steam- expIoded Pinus radiate. Biotechnol. Bioengery 3: 447–456. https://doi.org/10.1002/bit.260310509.Search in Google Scholar PubMed
Xiang, Q., Kim, J.S., and Lee, Y.Y. (2003). Kinetics of glucose decomposition during dilute-acid hydrolysis of lignocellulosic biomass. Appl. Biochemi. Biotechnol. 105: 337–352. https://doi.org/10.1385/abab:115:1-3:1127.10.1007/978-1-59259-837-3_91Search in Google Scholar
Yao, L., Chen, C., Zheng, X., Peng, Z., Yang, H., and Xie, Y., (2016). Determination of lignin–carbohydrate complexes structure of wheat straw using carbon-13 isotope as a tracer. BioResources 11: 6692–707. https://doi.org/10.15376/biores.11.3.6692-6707.Search in Google Scholar
Yokota, S., Iizuka, K., Ishiguri, F., Abe, Z., and Yoshizawa, N., (2006). Ozone–dioxane delignification from the cell walls of Japanese cypress (Chamaecyparis obtuse Endl.). J. Mater. Cycles Waste Manag. 8: 140–144. https://doi.org/10.1007/s10163-006-0149-6Corpus ID: 95043994.10.1007/s10163-006-0149-6Search in Google Scholar
You, T.T., Zhang, L.M., Zhou, S.K., and Xu, F. (2015). Structural elucidation of lignin–carbohydrate complex (LCC) preparations and lignin from Arundo donax Linn. Indus. Crops Prod. 71: 65–74. https://doi.org/10.1016/j.indcrop.2015.03.070.Search in Google Scholar
Zikeli, F., Ters, T., Fackler, K., Srebotnik, E., and Li, J. (2015). Wheat straw lignin fractionation and characterization as lignin–carbohydrate complexes. Indus. Crops Prod. 85: 309–317. https://doi.org/10.1016/j.indcrop.2016.03.012.Search in Google Scholar
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