Biodegradation and Sugar Release from Canola Plant Biomass by Selected White Rot Fungi

Omoanghe S. Isikhuemhen¹, Nona A. Mikiashvili¹, Zachary N. Senwo^2*, Elijah I. Ohimain³

¹Department of Natural Resources & Environmental Design, North Carolina A&T State University, Greensboro, USA.
²Department of Biological & Environmental Sciences, Alabama Agricultural & Mechanical University, Normal, USA.
³Niger Delta University, Wilberforce Island, Nigeria.

DOI: 10.4236/abc.2014.46045                

Abstract

Canola crop is rich in plant biomass. It is considered a major cash crop in North America and a potential source for biofuel. We evaluated six strains of white rot basidiomycetes under solid state fermentation (SSF) for their potentials to secrete oxidative and hydrolytic enzymes to biodegrade canola plant biomass (CPB), and release sugars. Fuscoporia gilva and Pleurotus tuberregium produced high amount of laccase (440.86 U/L and 480.63 U/L at day 7), as well as carboxylmethylcellulase (CMCase) (4.78 U/mL at day 21 and 3.13 U/mL at day 14) and xylanase (4.48 U/mL and 7.8 U/mL at day 21), respectively. Bjerkandera adusta showed high amount of MnP (50.4 U/L) and peroxidase (64.5 U/L), relative to the other strains. Loss of organic matter peaked after 21 days of incubation in all the tested strains; however, the best result (34.0%) was shown in P. tuberregium. The highest lignin loss was observed in Coriolopsis caperata strains. Among the sugar polymers, hemicellulose was highly degraded by P. tuberregium and P. pulmonarius (4.1% - 4.6%), while cellulose (3.3% - 4.3%) was mainly degraded by F. gilva and B. adusta. Glucose was the dominant sugar released by all the fungi tested, with the highest concentration of 1.25 mg/mL produced by B. adusta at day 14 of incubation. Results indicate that selected white rot fungi can achieve significant delignification of CPB within 14 days of solid state fermentation. Their importance in low cost pretreatment of lignocellulosic biomass prior to conversion into biofuels and bio-products of economic importance is discussed.

Keywords

Canola Plant Biomass, Bio-Delignification, White Rot Fungi, Lignocellulose

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	El Bassam, N. (2010) Handbook of Bioenergy Crops. Earthscan, Oxford, UK.
[2]	Blenis, P.V., Chow, P.S. and Stringam, G.R. (1999) Effects of Burial, Stem Portion and Cultivar on the Decomposition of Canola Straw. Canadian Journal of Plant Science, 79, 97-100. http://dx.doi.org/10.4141/P98-022
[3]	Adapa, P.K., Schoenau, G.J. Tabil, L.G., Sokhansanj, S. and Crerar, B.J. (2003) Pelleting of Fractionated Alfalfa Products. ASABE Paper No.036069, ASABE, St. Joseph.
[4]	Szczodrak, J. and Fiedukek, J. (1996) Technology for Conversion of Lignocellulosic Biomass to Ethanol. Biomass and Bioenergy, 10, 367-375. http://dx.doi.org/10.1016/0961-9534(95)00114-X
[5]	Wyman, C.E., Dale, B.E., Elander, R.T., Holtzapple, M., Ladisch, M.R. and Lee, Y.Y. (2005) Comparative Sugar Recovery Data from Laboratory Scale Application of Leading Pretreatment Technologies to Corn Stover. Bioresource Technology, 96, 2026-2032. http://dx.doi.org/10.1016/j.biortech.2005.01.018
[6]	Van Holme, R., Morreel, K., Ralph, J. and Boerjan, W. (2008) Lignin Engineering. Plant Biology, 11, 278-285.
[7]	Quiroz-Castaneda, R.E., Balcázar-López, E., Dantán-González, E., Martinez, A., Folch-Mallol, J. and Anaya, C.M. (2009) Characterization of Cellulolytic Activities of Bjerkandera adusta and Pycnoporus sanguineus on Solid Wheat Straw Medium. Microbial Biotechnology, 12. http://dx.doi.org/10.2225/vol12-issue4-fulltext-3
[8]	Zabel, R.A. and Morrell, J.J. (1992) Wood Microbiology: Decay and Its Prevention. Academic Press, London.
[9]	Kurt, S. and Buyukalaca, S. (2010) Yield Performances and Changes in Enzyme Activities of Pleurotus spp. (P. ostreatus and P. sajor-caju) Cultivated on Different Agricultural Wastes. Bioresource Technology, 101, 3164-3169. http://dx.doi.org/10.1016/j.biortech.2009.12.011
[10]	Isikhuemhen, O.S., Nerud, F. and Vilgalys, R. (2000) Cultivation Studies on Wild and Selected Hybrid Strains of Pleurotus tuberregium. World Journal of Microbiology and Biotechnology, 16, 431-435. http://dx.doi.org/10.1023/A:1008958319418
[11]	Salmones, D., Mata, G. and Waliszewski, K.N. (2005) Comparative Culturing of Pleurotus spp. on Coffee Pulp and Wheat Straw: Biomass Production and Substrate Biodegradation. Bioresource Technology, 96, 537-544. http://dx.doi.org/10.1016/j.biortech.2004.06.019
[12]	Akin, D.E., Rigsby, L.L., Sethuraman, A., Morrison, W.H., Gamble, G.R. and Eriksson, K.E.L. (1995) Alterations in Structure, Chemistry, and Biodegradability of Grass Lignocellulose Treated with the White Rot Fungi Ceriporiopsis subvermispora and Cyathus stercoreus. Applied and Environmental Microbiology, 61, 1591-1598.
[13]	Chen, J., Fales, S.L., Varga, G.A. and Royse, D.J. (1995) Biodegradation of Cell Wall Components of Maize Stover Colonized by White-Rot Fungi and Resulting Impact on in Vitro Digestibility. Journal of the Science of Food and Agriculture, 68, 91-98. http://dx.doi.org/10.1002/jsfa.2740680115
[14]	Karunanandaa, K., Varga, G.A., Akin, D.E., Rigsby, L.L. and Royse, D.J. (1995) Botanical Fractions of Rice Straw Colonized by White-Rot Fungi: Changes in Chemical Composition and Structure. Animal Feed Science and Technology, 55, 179-199. http://dx.doi.org/10.1016/0377-8401(95)00805-W
[15]	Koutrotsios, G., Mountzouris, K.C., Chatzipavlidis, I. and Zervakis, G.I. (2014) Bioconversion of Lignocellulosic Residues by Agrocybe cylindracea and Pleurotus ostreatus Mushroom Fungi—Assessment of Their Effect on the Final Product and Spent Substrate Properties. Food Chemistry, 161, 127-135. http://dx.doi.org/10.1016/j.foodchem.2014.03.121
[16]	Isikhuemhen, O.S., Mikiashvili, N.A., Adenipekun, C.O., Ohimain, E.I. and Shahbazi, G. (2012) The Tropical White Rot Fungus, Lentinus squarrosulus Mont: Lignocelluloytic Enzymes Activities and Sugar Release from Cornstalks under Solid State Fermentation. World Journal of Microbiology and Biotechnology, 28, 1961-1966. http://dx.doi.org/10.1007/s11274-011-0998-6
[17]	Sun, Y. and Cheng, J. (2002) Hydrolysis of Lignocellulosic Materials for Ethanol Production: A Review. Bioresource Technology, 83, 1-11. http://dx.doi.org/10.1016/S0960-8524(01)00212-7
[18]	Ohgren, K., Bura, R., Saddler, J. and Zacchi, G. (2007) Effect of Hemicelluloses and Lignin Removal on Enzymatic Hydrolysis of Steam Pretreated Corn Stover. Bioresource Technology, 98, 2503-2510. http://dx.doi.org/10.1016/j.biortech.2006.09.003
[19]	Ntougias, S., Baldrian, P., Ehaliotis, C., Nerud, F., Antoniou, T., Merhautová, V. and Zervakis, G.I. (2012) Biodegradation and Detoxification of Olive Mill Wastewater by Selected Strains of the Mushroom Genera Ganoderma and Pleurotus. Chemosphere, 88, 620-626. http://dx.doi.org/10.1016/j.chemosphere.2012.03.042
[20]	Wariishi, H., Valli, K. and Gold, M.H. (1991) In Vitro Depolymerization of Lignin by Manganese Peroxidase of Phanerochaete chrysosporium. Biochemical and Biophysical Research Communications, 176, 269-275. http://dx.doi.org/10.1016/0006-291X(91)90919-X
[21]	Gutiérrez, A., Martinez, M.J., Almendros, G., González-Vila, F.J. and Martinez, A.T. (1995) Hyphal-Sheath Polysaccharides in Fungal Deterioration. Science of the Total Environment, 167, 315-328. http://dx.doi.org/10.1016/0048-9697(95)04592-O
[22]	Catley, B.J. (1992) The Biochemistry of Some Fungal Polysaccharides with Industrial Potencial. In: Arora, D., Elander, R.P. and Mukerji, K.G., Eds., Handbook of Applied Mycology: Fungal Biotechnology, Marcel Dekker, New York, 259-279.
[23]	Sharma, R.K. and Arora, D.S. (2011) Biodegradation of Paddy Straw Obtained from Different Geographic Locations by Means of Phlebia spp. for Animal Feed. Biodegradation, 22, 143-152. http://dx.doi.org/10.1007/s10532-010-9383-7
[24]	Van Soest, P.J., Robertson, J.B. and Lewis, B.A. (1991) Methods for Dietary Fiber, Neutral Detergent Fiber, and Nonstarch Polysaccharides in Relation to Animal Nutrition. Journal of Dairy Science, 74, 3583-3597. http://dx.doi.org/10.3168/jds.S0022-0302(91)78551-2
[25]	Isikhuemhen, O.S. and Nerud, F. (1999) Preliminary Studies on the Ligninolytic Enzymes Produced by the Tropical Fungus Pleurotus tuber-regium (Fr.) Sing. Antonie van Leeuwenhoek, 75, 257-260. http://dx.doi.org/10.1023/A:1001871101604
[26]	Glenn, J.K. and Gold, M. (1983) Decolorization of Several Polymeric Dyes by the Lignin Degrading Basidiomycete, Phanerochaete chrysosporium. Applied and Environmental Microbiology, 45, 1741-1747.
[27]	Ghose, T.K. (1987) Measurement of Cellulase Activities. Pure and Applied Chemistry, 59, 257-268. http://dx.doi.org/10.1351/pac198759020257
[28]	Bailey, M.J., Biely, P. and Poutanen, K. (1992) Interlaboratory Testing of Methods for Assay of Xylanase Activity. Journal of Biotechnology, 23, 257-270. http://dx.doi.org/10.1016/0168-1656(92)90074-J
[29]	Poutanen, K. and Puls, J. (1988) Characteristics of Trichoderma reesei Beta-Xylosidase and Its Use in the Hydrolysis of Solubilized Xylans. Applied Microbiology and Biotechnology, 28, 425-432. http://dx.doi.org/10.1007/BF00268208
[30]	Quesada, A., Galvan, A. and Fernandez, E. (1994) Identification of Nitrate Transporters in Chlamydomonas reinhardtii. Plant Journal, 5, 407-419. http://dx.doi.org/10.1111/j.1365-313X.1994.00407.x
[31]	Hammel, K.E. (1997) Fungal Degradation of Lignin. In: Cadisch, G. and Giller, K.E., Eds., Driven by Nature: Plant Litter Quality and Decomposition, CAB International, Wallingford, 33-45.
[32]	Rois, S. and Eyzaguirre, J. (1992) Conditions of Selective Degradation of Lignin by the Fungus Ganoderma australis. Applied Microbiology and Biotechnology, 37, 667-669.
[33]	Rolz, C., De Leon, R., De Arriola, M.C. and De Cabrera, S. (1986) Biodelignification of Lemon Grass and Citronella Bagasse by White-Rot Fungi. Applied and Environmental Microbiology, 52, 607-611.
[34]	Mes-Hartree, M., Yu, E.K.C., Reid, I.D. and Saddler, J.N. (1987) Suitability of Aspenwood Biologically Delignified with Phlebia tremellosus for Fermentation to Ethanol or Butanediol. Applied Microbiology and Biotechnology, 26, 120-125. http://dx.doi.org/10.1007/BF00253894
[35]	Hatakka, A.I. (1983) Pretreatment of Wheat Straw by White-Rot Fungi for Enzymatic Saccharification of Cellulose. European Journal of Applied Microbiology and Biotechnology, 18, 350-357. http://dx.doi.org/10.1007/BF00504744
[36]	Mikiashvili, N.A., Isikhuemhen, O.S. and Ohimain, E.I. (2011) Lignin Degradation, Ligninolytic Enzymes Activities and Expolysaccharide Production by Grifola frondosa Strains Cultivated on Oak Sawdust. Brazilian Journal of Microbiology, 42, 1101-1108. http://dx.doi.org/10.1590/S1517-83822011000300031
[37]	Barrasa, J.M., Gutiérrez, A., Escaso, V., Guillén, F., Martínez, M.J. and Martínez, A.T. (1998) Electron and Fluorescence Microscopy of Extracellular Glucan and Aryl-Alcohol Oxidase during Wheat-Straw Degradation by Pleurotus eryngii. Applied and Environmental Microbiology, 64, 325-332.
[38]	Krcmar, P., Novotny, C., Marais, M.F. and Joseleau, J.P. (1999) Structure of Extracellular Poly-saccharide Produced by Lignin-Degrading Fungus Phlebia radiata in Liquid Culture. International Journal of Biological Macromolecules, 24, 61-64. http://dx.doi.org/10.1016/S0141-8130(98)00072-5
[39]	McCue, P.P. and Shetty, K. (2005) A Model for the Involvement of Lignin Degradation Enzymes in Phenolic Antioxidant Mobilization from Whole Soybean during Solid-State Bioprocessing by Lentinus edodes. Process Biochemistry, 40, 1143-1150.
[40]	Burns, P.J., Yeo, P., Keshavarz, T., Roller, S. and Evans, C.S. (1994) Physiological Studies of Exopolysaccharide Production from the Basidiomycete Pleurotus sp. florida. Enzyme and Microbial Technology, 16, 566-572. http://dx.doi.org/10.1016/0141-0229(94)90120-1
[41]	Maziero, R., Cavazzoni, V. and Bononi, V.L.R. (1999) Screening of Basidiomycetes for the Production of Exopolysaccharide and Biomass in Submerged Culture. Revista de Microbiologia, 30, 77-84. http://dx.doi.org/10.1590/S0001-37141999000100015
[42]	Elisashvili, V.I., Kachlishvili, E.T. and Wasser, S.P. (2009) Carbon and Nitrogen Source Effects on Basidiomycetes Exopolysaccharide Production. Applied Biochemistry and Microbiology, 45, 531-535. http://dx.doi.org/10.1134/S0003683809050135
[43]	Perera, P.K. and Li, Y. (2011) Mushrooms as a Functional Food Mediator in Preventing and Ameliorating Diabetes. Functional Foods in Health and Disease, 4, 161-171.
[44]	Lin, T.-C., Chang, J.-S. and Young, C.-C. (2008) Exopolysaccharides Produced by Gordonia alkanivorans Enhances Bacterial Degradation Activity for Diesel. Biotechnology Letters, 30, 1201-1206. http://dx.doi.org/10.1007/s10529-008-9667-8
[45]	Tien, M. and Kirk, T.K. (1983) Lignin-Degrading Enzyme from the Hymenomycete Phanerochaete chrysosporium Burds. Science, 221, 661-663. http://dx.doi.org/10.1126/science.221.4611.661
[46]	Tien, M. and Kirk, T.K. (1984) Lignin Degrading Enzymes from Phanerocheate chrysosporium: Purification, Characterization, and Catalytic Properties of a Unique H2O2 Requiring Oxygenase. Proceedings of the National Academy of Sciences of the United States of America, 81, 2280-2284. http://dx.doi.org/10.1073/pnas.81.8.2280
[47]	Kovacs, K., Macrelli, S., Szakacs, G. and Zacchi, G. (2009) Enzymatic Hydrolysis of Steam Pretreated Lignocellulisic Materials with Trichoderma atroviride Enzymes Produced In-House. Biotechnology for Biofuels, 2, 14-25. http://dx.doi.org/10.1186/1754-6834-2-14
[48]	Boominathan, K. and Reddy, C.A. (1992) cAMP-Mediated Differential Regulation of Lignin Peroxidase and Manganese-Dependant Peroxidase Production in the White Rot Basidiomycete Phanerochaete chrysosporium. Proceedings of the National Academy of Sciences of the United States of America, 89, 5586-5590. http://dx.doi.org/10.1073/pnas.89.12.5586
[49]	Duff, S.J.B. and Murray, W.D. (1996) Bioconversion of Forest Products Industry Waste Cellulosics to Fuel Ethanol: A Review. Bioresource Technology, 55, 1-33. http://dx.doi.org/10.1016/0960-8524(95)00122-0