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15 Fungal Biodegradation of Lignocelluloses 15 Fungal Biodegradation of Lignocelluloses 1 2 ANNELE HATAKKA ,KENNETH E. HAMMEL CONTENTS 2008). In Earth’s carbon cycle, especially in a for- I. Introduction ....................................... 319 est ecosystem, saprotrophic wood-decaying and II. Fungal Degradation of Lignocellulose ........... 320 litter-decomposing fungi perform an essential A. White-Rot Fungi . ...................... 320 role. Among them certain basidiomycetes, B. Brown-Rot Fungi. ...................... 321 so-called white-rot fungi, have a special role C. Soft-Rot Fungi. ................................ 321 III. Fungal Degradation of Wood since they are the only organisms that can effi- Polysaccharides.................................... 322 ciently degrade and even mineralize the most IV. Fungal Degradation of Lignin .................... 324 recalcitrant natural polymer, lignin. A. White-Rot and Brown-Rot Fungi . ............ 324 Cellulose is considered to be one of the most 1. Ligninolytic Peroxidases abundant biopolymers on Earth. It is the main of White-Rot Fungi. ................ 325 2. Peroxidases of Brown-Rot Fungi? . ...... 326 constituent of wood, and approximately 40% of 3. Laccases. .......................... 326 the dry weight of most wood species is cellulose, 4. Role of Small Oxidants in Incipient Decay 328 which is located predominantly in the secondary 5. Hydroquinones . .......................... 329 cell wall (Sjo¨stro¨m 1993). Cellulose is a homopo- 6. Cellobiose Dehydrogenases ................ 329 b 7. Redox-Active Glycopeptides . ...... 330 lysaccharide composed of -D-glucopyranoside B. Soft-Rot Fungi. ................................ 330 units which are linearly linked together by V. Biopulping as an Example of Potential (1!4)-glycosidic bonds. Cellulose can be crystal- Applications of White-Rot Fungi................. 331 line, sub-crystalline and even amorphous, depend- VI. Overview of Fungal Lignin Degradation and ing on the tissue source in native plant, or the way Outlook ............................................ 333 References.......................................... 335 that cellulose is isolated (Ding and Himmel 2008). The structural integrity of cellulose is one of the main obstacles of enzymatic hydrolysis of cellulose. For the isolation of cellulose harsh extraction I. Introduction methods involving sequential acid and alkaline treatments are usually employed. Fiber aggregation Wood and lignified gramineous and other annual caused by sample processing and found in isolated plants are generally called lignocellulose because cellulose does not necessarily represent the cellu- they are composed of the three main natural lose structure, and the detailed molecular structure polymers: cellulose, hemicelluloses and lignin. of plant cell wall cellulose remains unknown Lignocellulosic biomass is renewable, and huge (Ding and Himmel 2008). amounts of lignocellulose are annually synthe- Hemicelluloses in wood consist of relatively sized and degraded in nature. It has been esti- short, mainly branched heteropolymers of glu- mated that annual worldwide production of  12 cose, xylose, galactose, mannose and arabinose terrestrial biomass is 200 10 kg (Foust et al. as well as uronic acids of glucose, galactose and 4-O-methylglucose linked by (1!3)-, (1!6)- and (1!4)-glycosidic bonds. Galactoglucomannans are the principal hemicelluloses in softwoods, which also contain arabinoglucuronoxylan. 1 Department of Food and Environmental Sciences, University Xylose-based hemicelluloses are often termed of Helsinki, PO Box 56, Viikki Biocenter, 00014 Helsinki, Finland; e-mail: annele.hatakka@helsinki.fi xylans in both softwoods and hardwoods. 2USDA Forest Products Laboratory, One Gifford Pinchot Drive, Depending on hardwood species, the xylan con- WI 53726, Madison, USA; e-mail: [email protected] tent varies within the limits of 15-30% of the dry Industrial Applications, 2nd Edition The Mycota X M. Hofrichter (Ed.) © Springer-Verlag Berlin Heidelberg 2010 320 Annele Hatakka and Kenneth E. Hammel wood. Acetyl groups are present as substituents II. Fungal Degradation of Lignocellulose particularly in the glucomannans of gymnos- perms and the xylans of angiosperms (Sjo¨stro¨m A. White-Rot Fungi 1993). Hemicelluloses are reported to be linked to lignin through cinnamate acid ester linkages, to White-rot fungi are a heterogeneous group of fungi cellulose through interchain hydrogen bonding, that usually belong to basidiomycetes, although and to other hemicelluloses via covalent and there are ascomycetous fungi that cause pseudo- hydrogen bonds (Decker et al. 2008). white rot (also designated as soft-rot type II), such Lignin is a complex, amorphous, three-dimen- as fungi belonging to the family Xylariaceae sional aromatic polymer. Lignins are synthesized (Blanchette 1995; Liers et al. 2006). Basidiomyce- from the oxidative coupling of p-hydroxycinnamyl tous white-rot and some related litter-decomposing alcohol monomers, dimethoxylated (syringyl, S), fungi are the only organisms which are capable of monomethoxylated (guaiacyl, G) and non-meth- mineralizing lignin efficiently (Kirk and Cullen oxylated (p-hydroxyphenyl, H) phenylpropanoid 1998; Hatakka 2001). More than 90% of all wood- units. The molecular weight of lignin is difficult to rotting basidiomycetes are of the white-rot type determine because lignins are highly polydisperse (Gilbertson 1980). White-rot fungi are more com- materials (Argyropoulos and Menachem 1997). monly found on angiosperm than on gymnosperm New bonding patterns have been described in wood species in nature. Usually syringyl (S) units softwood lignin, e.g. dibenzodioxocin structures of lignin are preferentially degraded, whereas (Karhunen et al. 1995). Recent studies show that guaiacyl (G) units are more resistant to degrada- lignin can incorporate many more monolignols tion. Many white-rot fungi colonize cell lumina and than the traditional three basic units (Vanholme cause cell wall erosion. Eroded zones coalesce as et al. 2008), e.g. acetylated lignin units have been decay progresses and large voids filled with myce- identified in non-woody plants (Martı´nez et al. lium are formed. This type of rot is referred as 2005). The isolation of native lignin is complicated non-selective or simultaneous rot. Calcium oxalate if possible at all (Buswell and Odier 1987). Isolated and MnO2 accumulate when the decay proceeds lignin usually has a brown color but in sound (Blanchette 1995). Trametes (syn. Coriolus, Poly- non-degraded wood it is obviously colorless porus) versicolor is a typical simultaneous-rot because the wood of many tree species is almost fungus (Eriksson et al. 1990). Some white-rot white, and after attack by white-rot fungi, by fungi degrade lignin in woody plant cell walls rela- definition, the modified lignin in residual wood tively to a higher extent than cellulose, and they are and cellulose is also white. called selective white-rot fungi. In nature they may Uncertainties in the basic structures of espe- cause white-pocket or white-mottled types of rot, cially lignin but also other components in ligno- e.g. Phellinus nigrolimitatus (Blanchette 1995). cellulose make fungal biodegradation studies a There are also fungi, e.g. the tree pathogen Hetero- challenging task. The following properties are basidion annosum, that are able to produce both important in terms of microbial or enzymatic types of attack in the same wood (Eriksson et al. attack: (1) lignin polymers have compact struc- 1990). tures that are insoluble in water and difficult to penetrate by microbes or enzymes, (2) the In a screening to find suitable fungi for wood chip pre- intermonomeric linkages that account for the treatment for biopulping, 90 white-rot fungi were rigidity of lignin comprise many kinds of C–C cultivated in spruce (Picea abies) wood blocks for 10 and C–O bonds with the b-aryl ether linkage weeks, and about 20% of these fungi degraded more lignin than cellulose (Hakala et al. 2004). The selectivity depends being the most significant and (3) intermono- on the wood species, cultivation time, temperature and meric linkages in lignin are not hydrolyzable. many other things. This work and several other screening A conclusion from the above items is summarized studies have shown that e.g. Ceriporiopsis subvermispora, as follows: (1) polymeric lignin degradation Dichomitus squalens Phanerochaete chrysosporium, Phel- requires extracellular enzymes and/or small linus pini, Phlebia radiata, Phlebia tremellosus (syn. Mer- ulius tremellosa), Phlebia subserialis, Physisporinus molecular weight mediators or factors such as rivulosus, Pleurotus eryngii, Pleurotus ostreatus and Pyc- radicals, (2) the lignin degrading system must be noporus cinnabarinus are lignin-selective fungi at least unspecific and (3) the enzymes must be oxidative, under certain conditions (Eriksson et al. 1990; Akhtar not hydrolytic. et al. 1998; Hatakka 2001; Hakala et al. 2004). Fungal Biodegradation of Lignocelluloses 321 B. Brown-Rot Fungi polysaccharides involves not only hydrolytic enzymes, but also an oxidative component (Kirk Brown-rot fungi are basidiomycetes that degrade et al. 1991). Analyses of lignin from brown-rotted wood to yield brown, shrunken specimens that wood have likewise shown that it becomes oxi- typically exhibit a pattern of cubical cracks dized, partially via demethylation of the aromatic and easily disintegrate upon handling. Only a rings, which increases the phenolic hydroxyl con- small proportion – roughly 7% – of all wood tent, and
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