Lignin Biodegradation by Selective White Rot Fungus and Its Potential

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Chapter 26

Lignin Biodegradation by Selective White Rot Fungus and Its Potential Use in Wood Biomass Conversion 1

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T. Watanabe, Y. Ohashi , T. Tanabe , Y. Honda , and K. Messner 1

Laboratory of Biomass Conversion, Research Institute for Sustainable Humanosphere (RISH), Kyoto University, Gokasho, Uji, Kyoto 611-0011, Japan Laboratory of Industrial Microbiology, Institute for Bioengineering, University of Technology, Vienna, Austria 2

A selective white rot fungus, Ceriporiopsis subvermispora is shown to, degrade lignin without extensive damage to cellulose. This selective ligninolysis reaction is catalyzed by low molecular mass compounds at a site far from the enzymes. At an incipient stage of the wood decay, the fungus catalyzed in situ lipid peroxidation and secreted alkylitaconic acids and ceriporic acids. The extracellular metabolites are thought to attenuate the iron redox reactions, thereby inhibiting the production of a cellulolytic active oxygen species such as hydroxyl radicals. The selective lignolysis by this fungus can be applied to pretreatments of wood for ethanol fermentation, methane fermentation and feedstuff production.

© 2007 American Chemical Society

In Materials, Chemicals, and Energy from Forest Biomass; Argyropoulos, D.; ACS Symposium Series; American Chemical Society: Washington, DC, 2007.

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Introduction The continued use of fossil fuels is a serious environmental problem, causing the emission of carbon dioxide. In order to avoid serious global warming by the emission of carbon dioxide from fossil fuels, there is a growing demand for the production of energy and chemicals from renewable resources. In order to convert wood biomass by enzymatic saccharification and fermentation, the degradation of the lignin network is necessary because the cell wall polysaccharides are covered with lignin in the lignified plant cell walls. One potential approach to degrade lignin prior to saccharification and fermentation is to use the ligninolytic systems of white rot fungi. Among the numerous fungi so far isolated, a white rot fungus, Ceriporiopsis subvermispora is characterized as being highly potent toward biopulping, degrading lignin without extensive damage of cellulose " . Previous studies revealed that the selective ligninolysis by this fungus is catalyzed by low molecular mass compounds at a site far from the extracellular enzymes and fungal hyphae " . This fungus has been shown to decompose non-phenolic lignin model compounds . In this chapter, the lipidrelated extracellular metabolites of C subvermispora and the conversion of wood biomass into ethanol, methane and other materials is reviewed. (1

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Control of Active Oxygen Species and Radicals by Extracellular Lipid-Related Metabolites The biodégradation of lignin is an extracellular free radical event that proceeds in concert with the activation of molecular oxygen and redox cycling of transition metals. When wood is colonized by wood-degrading fungi, their extracellular enzymes are not able to diffuse into the intact wood cell walls because the enzymes are too large to penetrate their pores. Hydroxyl radicals, (•OH), a radical species highly destructive to cellulose and lignin model compouds ' , is proposed as a principal low molecular mass oxidant that erodes wood cell walls to enhance the accessibility of the extracellular enzymes of wood rot fungi to the components of wood cell walls. In brown rot, hydroxyl radicals disrupt cellulose and hemicelluloses in wood cell walls, with concomitant modification of lignin substructures like demethoxylation and hydroxylation of aromatic rings " . The production of hydroxyl radicals are also reported for non-selective white rot fungi ' . Hydroxyl radicals are produced by the reaction of F e with H 0 (Fenton reaction; F e + H 0 -> F e + OH" + -OH), although other transition metals like Cu are able to participate in the production of ·ΟΗ. In the Fenton system, catalysts for the reductive half cycle ( F e - * Fe ) accelerate the hydroxyl radical formation. Wood rot fungi have versatile 7 8)

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411 enzymatic and non-enzymatic systems to accelerate the reductive half cycle. ' ' " * In contrast to brown rot and non-selective white rot fungi, selective lignindegrading fungi like Ceriporiopsis subvermispora are able to decompose lignin in wood cell walls without the intensive damage of cellulose. Wood decay by the biopulping fungus proceeds without the penetration of extracellular enzymes into the wood cell wall regions *. Lipid peroxidation has been proposed as a major pathway for the ligninolysis of this fungus at an incipient stage of wood decay " *. Lignin biodégradation proceeds by free radical process in the presence of molecular oxygen and transition metals. Reductive radicals such as semiquinone radical reduce molecular oxygen to produce superoxide, which in turn reduce F e or disproportionate into H 0 . F e is directly reduced by lignin-derived phenols such as guaiacol and catechol *. Thus, i f some inhibition systems for the iron redox reactions were not involved in the wood decaying systems, production of the cellulolytic oxidant, hydroxyl radical is inevitable (Fig. 1). This strongly suggests that the selective white rot fungus possesses unknown extracellular systems that attenuate tfye production of hydroxyl radicals. 8 11 13

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Figure 1. A proposedpathway for the generation ofhydroxyl radicals (·ΟΗ) during lignin biodégradation by nonselective white rotfungi. Phenols and reductive radical species reduce Fe to promote the Fenton reaction. Wood cell walls are eroded by the hydroxyl radicals to assist penetration of extracellular enzymes. 3+



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Figure 2. A proposed pathway for the inhibition of hydroxyl radicals (·0Η) by the selective white rot fungus, Ceriporiopsis subvermisopora. The fungus secretes ceriporic acids. The metabolites inhibit production of a cellulolytic active oxygen species, hydroxyl radical by suppressing iron redox reactions.

First, a series of novel itaconic acid derivatives having a long alkyl side chain at position C-3 o f its core (ceriporic acids) were.isolated from the cultures of C. subvermisrpora ' \ Gutierrez at al. reported the same compounds by G C M S analysis of crude extracts from eucalypt wood decayed by C. subvermisrpora, Phlebia radiata, Pleurotus pulmonarius, and Bjerkandera adusta in 2002 . Dodecanyl-, tridecanyl-, tetradecenyl-, pentadecanyl-, octadecenyl- and octadecanylitaconic acids, were also detected in very minor amounts or traces by the G C M S analysis of eucalypt wood cultures *. It was reported that the alkylitaconic acid strongly suppressed the Fenton reactions even in the presence of the F e reductants such as cysteine and hydroquinone * (Fig. 2). The inhibition of · Ο Η production by the diffusible fungal metabolite accounts for the extracellular system of the fungus that attenuates the formation of · Ο Η in the presence of iron, molecular oxygen and free radicals produced during lignin biodégradation. Recently, it was reported 25 27

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Reaction Time / h

Figure 3. Ceriporic acid B, an extracellular metabolite of C. subvermispora suppresses the depolymerization of cellulose by the Fenton reaction: U)

that l-nonadecene-2,3-dicarboxylic acid (ceriporic acid B ) , an extracellular metabolite of C. subvermispora, strongly inhibited · Ο Η production and the depolymerization of cellulose by the Fenton reaction in the presence of iron ions, cellulose, H 0 and a reductant for F e , hydroquhione (HQ), at the physiological p H of the fiingus (Fig. 3). A s expected by the in vitro experiments, this metabolite may play a key role in the mechanism o f selective white rot because a high level of production of alkylitaconic acids has been observed only for C. subvermispora in SSF cultures of four white-rot fungi, C. subvermisrpora, Phlebia radiata Pleurotus pulmonarius and Bjerkandera adusta *\ In the incipient stage of wood decay, this fungus produced saturated (SFAs) and unsaturated fatty acids (USFAs), including linoleic acid (18:2n-6),and oxidized them with manganese peroxidase (MnP) to produce hydroperoxides and T B A R S . The lipid peroxidation with M n P has been proposed as a ligninolytic system o f this fungus because diffusible M n chelates can react with lipid and lipid hydroperoxides to generate free radicals *. Analysis of the catalytic mechanisms of MnP for lipid peroxidation of linoleic acid revealed that the reaction starts from hydrogen abstraction from the enolic form of the fatty 3+

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414 acids and proceeds by acyl radical chain reaction, accompanied by the production of aldehydes including glyoxal . When free radicals were produced from lipid hydroperoxide models, T B H P or C H P with copper complexes, nonphenolic synthetic lignin was depolymerized , and both softwood and hardwood were delignified, leading to fiber separation, as observed in selective white rot . The copper system was applied to biomimetic bleaching of p u l p , and it is potentially applicable to pretreatments of wood for enzymatic saccharification and fermentation. The reactions were carried out by mixing 0.5 m M FeCl , 0.25 m M HQ, 100 m M H 0 and 0.1 g cellulose in the presence and absence of 2.5 m M ceriporic acid B. Control contained cellulose and H 0 . 23)

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Conversion of Wood Biomass Using Selective White Rot Fungi The development of conversion systems from lignocellulosics into biofuels and chemicals has received much attention due to immense potentials for the utilization of renewable bioresources. For example, ethanol production from lignocellulosics has been examined by saccharification with acids or cellulolytic enzymes and subsequent ethanol fermentation with yeast or gene-engineered bacteria. Since lignin makes the access of cellulolytic enzymes to cellulose difficult, it is necessary to decompose the network of lignin prior to enzymatic hydrolysis. Thus, effective pretreatments are needed for enzymatic saccharification and ethanol production from lignocellulosics. Biological pretreatment with lignin-degrading fungi is one possible approach (Fig. 4). It was reported that ethanol was produced by simultaneous saccharification and fermentation (SSF) from beech wood chips after bioorganosolve pretreatments by ethanolysis and white rot fungi, C. subvermispora, Dichomitus squalens, Pleurotus ostreatus, and Coriolus versicolor^. Beech wood chips were pretreated with the white rot fungi for 2-8 weeks without addition of any nutrients. The wood chips were then subjected to ethanolysis to separate them into pulp and soluble fractions (SFs). From the pulp fraction (PF), ethanol was produced by SSF using Saccharomyces cerevisiae A M 12 and a commercial cellulase preparation, Meicelase, from Trichoderma viride. Among the four strains, C subvermispora gave the highest yield on SSF. The yield of ethanol obtained after pretreatment with C. subvermispora for 8 weeks was 0.294 g g" of ethanolysis pulp (74% of theoretical) and 0.176 g g" of beech wood chips (62% of theoretical). The yield was 1.6 times higher than that obtained without the fungal treatments. The biological pretreatments saved 15% of the electricity needed for the ethanolysis. 1

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Treatments with white rot fungi were also applied to the production of feed for ruminants from Japanese cedar wood . Japanese cedar wood chips were 37)



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Figure 4. Production of ethanol methane, feedstuff and other useful chemicals from biomass using pretreatments with selective white rot fungi.

treated with white rot fungi, Pleurotus ostreatus, L. edodes, Pholiota nameko, Dichomitus squalens and C. subvermispora (Fig. 5). In order to determine the digestibility of the wood, in vitro organic matter digestibility (IVOMD) and in vitro gas production (IVGP) were measured. The solubilization of the wood by the rumen microorganisms can be evaluated by I V O M D , and anaerobic fermentation via volatile fatty acid ( V F A ) production can be estimated by IVGP. Because increase in I V O M D is not proportional to the amount of organic matter (OM) available as an energy source for ruminants, measurement of IVGP is important to evaluate the digestibility. In vitro organic matter digestibility (IVOMD) in Japanese cedar wood without fungal treatments was between 0.047 and 0.068, while it was elevated to 0.446 by culturing with C. subvermispora for 20 weeks. The in vitro gas production (IVGP) in Japanese cedar wood cultured with C. subvermispora for 20 weeks increased to 107 ml/g organic matter (OM), while I V G P for P. ostreatus, Ρ nameko or D. squalens was 37 ml/g O M , or lower. These results demonstrate that C. subvermispora has the highest potential to convert Japanese cedar wood into a feed for ruminants. The pretreatments with white rot fimgi were applied to methane fermentation from Japanese cedar wood (Fig. 6) . Methane fermentation is advantageous for on-site energy supply. Methane gas can be converted to electricity using fuel cells or turbine systems, or combusted directly. The * development of a bioconversion system from wood to methane should accelerate the establish ment of bioenergy-based societies that use wood and forestry wastes to make electricity, heat and fuels. Fungal pretreatments were studied with 38)


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C. subvermispora S

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C. subvermispora ~ 100.0

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Figure 5. The change in in vitro organic matter digestibility (IVOMD) and in vitro gas production (IVGP) (ml/g organic matter) of Japanese red cedarwood cultured with basidiomycetes for different culture lengths. (Reproduced with permission from reference 37. Copyright 2005 Elsevier.)



417 several strains of C subvermispora and Pleurocybella porrigens for methane fermentation of Japanese cedar wood. The methane fermentation of Japanese cedar wood was carried out after pretreatment with four strains of white rot fungi, Ceriporiopsis subvermispora A T C C 90467, CZ-3, C B S 347.63 and Pleurocybella porrigens K-2855. These fungi were cultivated on wood chip media with and without wheat bran for 4-8 weeks. The pretreated wood chips were fermented anaerobically with sludge from a sewage treatment plant. Pretreatments with C subvermispora A T C C 90467, CZ-3 and C B S 347.63 in the presence of wheat bran for 8 weeks decreased 74-76% of beta aryl ether linkages in the lignin to accelerate production of methane. After fungal treatments with C subvermispora A T C C 90467 and subsequent 30-day methane fermentation, the methane yield reached 35% and 25% of the theoretical yield based on the holocellulose contents of the decayed and original wood, respectively. In contrast, treatment with the three strains of C subvermispora without wheat bran cleaved 15-26% of the linkage and produced 6-9% of methane. There were no significant accelerating effects in wood chips treated with P. porrigens which has a lower ability to decompose the lignin. Thus, it was found that C. subvermispora with a high ability to decompose aryl ether bonds of lignin, promoted methane fermentation of softwood in the presence of wheat bran. Studies on the lignin biodégradation by selective white rot fungi will provide new insights into the development of environmentally-friendly processes for the production of chemicals, fuels and eco-materials from wood and nonwood lignocellulosics.

Conclusions A selective white rot fungus, C subvermispora, is able to delignify wood without penetration of extracellular enzymes into wood cell wall regions. The fungus has been applied to biopulping, and the production of feedstuff, ethanol and methane. In the incipient stage of wood decay, this fungus produces saturated and unsaturated fatty acids including linoleic acid. Subsequently oxidizing them with MnP generating free radicals. During the wood decay process, this fungus produces a series of alkylitaconic acids called ceriporic acids. In vitro experiments demonstrated that ceriporic acid Β intensively inhibited ·ΟΗ production by the Fenton reaction by suppressing the iron redox cycle. The fungal metabolite suppressed cellulose degradation by the Fenton reaction even in the presence of reductants for F e at the physiological p H of the fungal decay. 3+


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Control C. subvermtspora C. subvermispora C. subvermispora ATCC 90467 CZ-3 CBS 347.63

P. porrigens K-2855

Figure 6. Conversion ratio of holocellulose of Japanese cedar wood to methane and after fungal pretreatments for 8 weeks and subsequent methane fermentation for 30 days. Values are expressed as percentage based on the weight of holocellulose in the original wood. (Reproduced with permission from reference 34. Copyright 2002 Elsevier.)

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421 29. del Rio, J. C.; Gutiérrez, Α.; Martinéz, M. J.; Martinéz, A.T. Identification of a novel series of alkylitaconic acids in wood cultures of Ceriporiopsis subvermispora by gas chromatography/mass spectrometry. Rapid Commun. Mass Spectrom. 2002, 16, pp 62-68. 30. Watanabe, T.; Teranishi, H . ; Honda, Y.; Kuwahara, M. A selective lignindegrading fungus, Ceriporiopsis subvermispora produces alkylitaconates that inhibit the production of a cellulolytic active oxygen species, hydroxyl radical in the presence of iron and H O . Biochem. Biophys. Res. Commun. 2002, 297, pp 918-923. 31. Rahmawati, N.; Ohashi, Y . ; Watanabe, T.; Honda, Y . ; Watanabe, T. Ceriporic acid B , an extracellular metabolite of Ceriporiopsis subvermispora suppresses the depolymerization of cellulose by the Fenton reaction. Biomacromolecules 2005, 6, pp 2851-2856. 32. Watanabe, T.; Koller, K . ; Messner, K . Copper-dependent depolymerization of lignin in the presence of fungal metabolite, pyridine. J. Biotechnol. 1998, 62, pp 221-230. 33. Messner, K . ; Fackler, K.; Lamaipis, P.; Gindl, W.; Srebotnik, E.; Watanabe, T. Overview of White-Rot Research: Where we are today. ACS Symposium Series 845 Wood deterioration and preservation, American Chemical Society: Washington, DC, 2003; pp 73-96. 34. Fackler, K . ; Srebotnik, E.; Watanabe, T.; Lamaipis, P.; Humar, M.; Tavzes, C.; Sentjurc, M.; Pohleven, F.; Messner, K . Biomimetic pulp bleaching with copper complexes and hydroperoxides, Biotechnology in the Pulp and Paper Industry, Progress in Biotechnology V o l 21, L . Viikari and R. Lantto, Eds.; Elsevier, Amsterdam, 2002; pp 223-230. 35. Rahmawati, N.; Ohashi, Y.; Honda, Y.; Kuwahara, M.; Fackler, K . ; Messner, K . ; Watanabe, T. Pulp bleaching by hydrogen peroxide activated with copper 2,2'-dipyridylamine and 4-aminopyridine complexes. Chem. Eng. J. 2005, 112, pp 167-171. 36. Itoh H . ; Wada, M . ; Honda, Y . ; Kuwahara, M . ; . Watanabe, T. Bioorganosolve pretreatments for simultaneous saccharification and fermentation of beech wood by ethanolysis and white rot fungi. J. Biotechnol. 2003, 103, pp 273-280. 37. Okano, K . ; Kitagawa, M.; Sasaki, Y . ; Watanabe, T. Conversion of Japanese red cedar (Cryptomeria japonica) into feed for ruminants by white-rot basidiomycetes. Animal Feed Sci. Technol. 2005, 120, pp 235-243. 38. Amirta R.; Tanabe, T.; Watanabe, T.; Honda, Y . ; Kuwahara, M. Watanabe, T. Methane fermentation of Japanese cedar wood pretreated with a white rot fungus, Ceriporiopsis subvermispora. J. Biotechnol., 2006, in press. 2

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Lignin Biodegradation by Selective White Rot Fungus and Its Potential

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