Extracellular Peroxidases Involved in Lignin Degradation by the White

Chapter 9

Extracellular Peroxidases Involved in Lignin Degradation by the White Rot Basidiomycete

Phanerochaete

chrysosporium

Michael H. Gold, Hiroyuki Wariishi, and Khadar Valli

Downloaded by UNIV OF SYDNEY on September 13, 2013 | http://pubs.acs.org Publication Date: January 1, 1989 | doi: 10.1021/bk-1989-0389.ch009

Department of Chemical and Biological Sciences, Oregon Graduate Center, Beaverton, OR 97006-1999 The white rot basidiomycete Phanerochaete chrysosporium secretes two soluble H O -requiring peroxidases which are involved i n l i g n i n degradation. Both l i g n i n peroxidase (LiP) and manganese peroxidase (MnP) form the oxidized intermediates compound I and compound I I . LiP catalyzes the one-electron oxidation of a variety of substrates to generate a r y l cation r a d i c a l s . These radicals undergo subsequent nonenzymic reactions to y i e l d a m u l t i p l i c i t y of f i n a l products. MnP oxidizes MnII to MnIII which acts as a unique redox couple, and in turn oxidizes phenolic substrates to phenoxy radicals, which undergo subsequent reactions to y i e l d the f i n a l products. 2

2

Lignin i s the second most abundant natural polymer i n the biosphere and the most abundant renewable aromatic material. I t comprises 1530% of woody plant c e l l walls, forming a matrix surrounding the c e l l u l o s e . This encrusting matrix (1,2) s i g n i f i c a n t l y retards the microbial depolymerization of c e l l u l o s e and thus l i g n i n plays a key role i n the earth's carbon cycle (1-3). Lignin i s a phenylpropanoid polymer (Fig. 1) synthesized from phydroxycinnamyl (coumaryl) alcohol, 4-hydroxy-3-methoxycinnamyl (coniferyl) alcohol and 3,5-dimethoxy-4-hydroxycinnamyl (sinapyl) alcohol precursors (2,3). Free r a d i c a l condensation of these alcohols, i n i t i a t e d by plant c e l l wall peroxidases, results in the formation of a heterogeneous, amorphous, o p t i c a l l y inactive, random and highly branched polymer containing a t l e a s t 12 d i f f e r e n t interunit linkages connecting the aromatic nuclei. The most abundant linkage i s the 3-0-4 type (between aromatic nuclei 2 and 1 i n F i g . 1). The 3-1 linkage type (between aromatic nuclei 11 and 12 i n F i g . 1) has served as a model i n several biodégradation studies. White-rot basidiomycetes are the only known organisms which are capable of degrading l i g n i n extensively to C0 and H 0 i n pure culture. These organisms invade the lumen of woody plant c e l l s and secrete e x t r a c e l l u l a r enzymes which attack a l l of the polymers i n 2

2

0097-6156/89/0389-0127$06.00/0 ° 1989 American Chemical Society

In Biocatalysis in Agricultural Biotechnology; Whitaker, J., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1989.


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BIOCATALYSIS IN AGRICULTURAL BIOTECHNOLOGY

Figure 1.

Schematic structure for conifer l i g n i n .



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GOLD ET A L

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Peroxidases Involved in Lignin Degradation

wood. E a r l y work I n d i c a t e d t h a t l i g n i n d e g r a d a t i o n by the b e s t s t u d i e d l i g n i n d e g r a d i n g fungus, Phanerochaete c h r y s o s p o r i u m , i s o x i d a t i v e and n o n s p e c i f i c ( 4 - 6 ) . Chemical a n a l y s e s o f w h i t e - r o t t e d r e s i d u a l l i g n i n (7,8) and o f l i g n i n model compound d e g r a d a t i o n p r o d u c t s (9-11) i n d i c a t e d t h a t s i d e c h a i n c l e a v a g e and r i n g opening r e a c t i o n s occur simultaneously. S i n c e l i g n i n i s such a c o m p l i c a t e d i n s o l u b l e polymer, i t i s d i f f i c u l t to e l u c i d a t e the mechanism o f i t s o x i d a t i o n by a n a l y s i s o f i t s d e g r a d a t i o n p r o d u c t s . T h e r e f o r e , s t a r t i n g i n the l a t e 1970*8, a number o f s t u d i e s i n our own l a b o r a t o r y and from the l a b o r a t o r i e s o f T. H i g u c h i and T. K. K i r k f o c u s e d on the metabolism o f d i m e r i c model l i g n i n s u b s t r u c t u r e s ( 9 - 1 6 ) , whose o x i d a t i o n p r o d u c t s a r e e a s i e r to a n a l y z e than the d e g r a d a t i o n fragments o f the p o l y m e r i c s u b s t r a t e . D i m e r i c model compounds were shown to be degraded under the same p h y s i o l o g i c a l c o n d i t i o n s n e c e s s a r y f o r polymer d e g r a d a t i o n (4,5,121 8 ) , s u g g e s t i n g t h a t the l i g n i n d e g r a d a t i o n system was r e s p o n s i b l e f o r the o x i d a t i o n o f these model compounds. Work w i t h 3-0-4 and 3-1 d i m e r i c model compounds i n d i c a t e d t h a t a m u l t i p l i c i t y o f o x i d a t i v e r e a c t i o n s were c a t a l y z e d by the n o n s p e c i f i c l i g n i n dégradative system of c h r y s o s p o r i u m (9-17). Indeed, the m e t a b o l i c s t u d i e s w i t h d i m e r i c l i g n i n model compounds l e d to the r a t i o n a l d e s i g n o f a s s a y s f o r the enzymic components o f the l i g n i n dégradative system. I n 1983, our l a b o r a t o r y and t h a t o f T. K. K i r k announced the simultaneous d i s c o v e r y i n c h r y s o s p o r i u m o f an e x t r a c e l l u l a r H 0 r e q u i r i n g enzyme i n v o l v e d I n l i g n i n d e g r a d a t i o n (19-22). T h i s enzyme i s now r e f e r r e d to as l i g n i n p e r o x i d a s e ( L i P ) o r l i g n i n a s e . Subseq u e n t l y , a second P. c h r y s o s p o r i u m enzyme i n v o l v e d i n l i g n i n degradat i o n , manganese p e r o x i d a s e (MnP), was i s o l a t e d i n our l a b o r a t o r y (23). These two enzymes, L i P and MnP, a l o n g w i t h an H 0 g e n e r a t i n g system (24) appear to be the major components o f the £. c h r y s o s p o r i u m l i g n i n d e g r a d a t i o n system. T h i s c h a p t e r r e v i e w s some o f the work on the s p e c t r o s c o p i c and m e c h a n i s t i c p r o p e r t i e s o f these p e r o x i d a s e s . For more e x h a u s t i v e r e v i e w s o f l i g n i n d e g r a d a t i o n , see L i t e r a t u r e C i t e d (24,25). 2

2

2

2

L i g n i n P e r o x i d a s e and Manganese P e r o x i d a s e ; G e n e r a l P r o p e r t i e s L i P has been p u r i f i e d to e l e c t r o p h o r e t i c homogeneity by a c o m b i n a t i o n o f a n i o n exchange chromatography and g e l f i l t r a t i o n (26-28). The enzyme i s p r e s e n t as a s e r i e s o f isozymes (28,29) w i t h p i r a n g i n g from 3.2 to 4.0. L i P c o n t a i n s one mole o f i r o n p r o t o p o r p h y r i n IX per mole o f enzyme and i s a g l y c o p r o t e i n o f m o l e c u l a r mass 41,000. MnP has a l s o been p u r i f i e d to e l e c t r o p h o r e t i c homogeneity (30,31). The enzyme e x i s t s as a s e r i e s o f isozymes w i t h p i r a n g i n g from 4.2 to 4.9, c o n t a i n s one mole o f i r o n p r o t o p o r p h y r i n IX per mole o f enzyme and i s a g l y c o p r o t e i n o f m o l e c u l a r mass 46,000 (29-31). S p e c t r o s c o p i c P r o p e r t i e s o f L i g n i n P e r o x i d a s e and Manganese Peroxidase E l e c t r o n i c a b s o r p t i o n maxima f o r L i P , MnP, h o r s e r a d i s h p e r o x i d a s e (HRP) and v a r i o u s l i g a n d e d forms o f these enzymes a r e shown i n T a b l e I . The s p e c t r a o f n a t i v e L i P and MnP a r e c h a r a c t e r i s t i c o f h i g h - s p i n f e r r i c heme p r o t e i n s , w i t h S o r e t and v i s i b l e maxima ( 407, 502 and


130


632) (26,30) similar to those of HRP and myoglobin. Like HRP, the f e r r i c forms of LiP and MnP form typical low-spin hexacoordinate complexes with CN" and Ν ~ (26,30), with spectra d i s t i n c t from those of P-450 low-spin complexes (32). The spectra of the reduced enzymes are typical of high-spin pentacoordinate ferrous heme. The ferrous enzymes also form complexes with CO (Table I) which have spectra typical of peroxidases and rule out a cysteinate f i f t h ligand as i s found i n cytochrome P-450 (32,33). 3


Table I.

Electronic Absorption Spectral Maxima of Lignin Peroxidase, Manganese Peroxidase, and Horseradish Peroxidase

Ref.

Sys tem

Ferric, LiP, MnP, HRP,

high spin pH 4.5 pH 4.5 pH 6.0

407 406 403

632 632 641

500 502 500

26 30 39

F e r r i c , low spin CN"-LiP

423

540

26

CN"-MnP

421

546

30

CN--HRP

422

539

39

N "-LiP

418

540

575

26

Ν

"-MnP

417

542

580

30

Ν

"-HRP

565

39

3

416

534

Ferrous LiP MnP HRP

435 433 437

556 554 556

Ferrous CO CO-LiP CO-MnP CO-HRP

420 423 423

535 541 541

26 30 39

568 570 575

26 30 39

The EPR spectra of native LiP (34) and MnP (35) are also typical of high-spin f e r r i c heme, with g values 5.83 and 1.99 (LiP) and 5.79 and 1.99 (MnP). These values are e s s e n t i a l l y i d e n t i c a l to those of aquometmyoglobin but d i f f e r somewhat from those of HRP for which a large rhombic component i s observed. Resonance Raman (RR) studies (34-37) also indicate that native LiP and MnP are high-spin f e r r i c enzymes which are predominantly pentacoordinate at room temperature. RR studies confirm that the native enzymes form low-spin complexes with CN~ and N ~ and that the reduced enzymes have high-spin 3



9. GOLD ET AL.

131

pentacoordinate ferrous hemes. A l l of these studies Indicate that the f i f t h llgand to the heme iron i s a h i s t l d i n e as found f o r other plant peroxidases (38,39). Oxidized Intermediates of LIP and MnP Optical spectral data for the oxidized intermediates of LiP, MnP and HRP are shown i n Table II (38-41). The primary reaction product of peroxidases with H 0 i s the oxidized intermediate compound I. This intermediate has absorption maxima a t ~ 4 0 7 , ~550 and ~650 (Table I I ) . The absorption maxima of LiP and MnP compounds I are very s i m i l a r to those of HRP compound I, Indicating that they contain two oxidizing equivalents over the native f e r r i c enzyme. The f i r s t oxidizing equivalent resides In the F e l V O state of the Iron (38,39). The second equivalent resides i n a porphyrin π-cation r a d i c a l [PÎ]. Reduction of compound I by one molar equivalent y i e l d s compound II (maxima a t ~420, ~525 and ~555). A variety of spectroscopic studies indicate an FeIV=0 structure for HRPII (38,39). Recent RR evidence supports an FeIV=0 structure for LiPII (36). F i n a l l y , addition of excess H 0 to HRP, LiP or MnP y i e l d s the complex compound I I I (maxima ~419, 545, 579) which i s believed to be a f e r r i c superoxide complex (FeIII0 ~) (39-41). While compound I I I i s not part of the normal c a t a l y t i c cycle of peroxidases, L i P i s unusual i n that i t i s e a s i l y oxidized to LiPIII a t i t s pH optimum (3.0) In the absence of reducing substrate. This r e s u l t s i n the i n a c t i v a t i o n of the enzyme (Wariishi and Gold, In preparation, 42).


2

2

2

2

2

Table I I .

Peroxidase

LiP MnP HRP

Absorption Maxima (nm) of Oxidized of Several Peroxidases

Compound I

Compound III

Compound II

408, 550, 608, 650 407, 558, 605, 650 400, 557, 622, 650

420, 420, 420,

Intermediates

525, 556 528, 555 527, 554

419, 417, 413,

543, 578 545, 579 546, 583

Ref.

40 41 38,39

Lignin Peroxidase Kinetics and C a t a l y t i c Cycle LiP catalyzes the oxidation of 3,4-dimethoxybenzyl alcohol ( v e r a t r y l alcohol) to v e r a t r y l aldehyde. Since this reaction can be e a s i l y followed a t 310 nm, i t i s the basis for the standard assay f o r this enzyme (26,27). The enzyme exhibits normal saturation k i n e t i c s for both v e r a t r y l alcohol and H 0 (28,43). Steady-sta te k i n e t i c results indicate a ping-pong mechanism i n which H 0 f i r s t oxidizes the enzyme and the oxidized Intermediate reacts with veratryl alcohol (43). The enzyme has an extremely low pH optimum (~2.5) for a peroxidase (43,44); however, the rate of formation of compound I ( k , Fig. 2) exhibits no pH dependence from 3.0-7.0 (45,46). Addition of excess v e r a t r y l alcohol a t pH 3.0 results i n the rapid conversion of 2

2

2

2

x


132

BIOCATALYSIS IN AGRICULTURAL

BIOTECHNOLOGY

L i P I to L i P I I (~20 msec) f o l l o w e d by a s l o w e r c o n v e r s i o n o f L i P I I to the n a t i v e enzyme (~500 msec) ( 4 6 ) . Thus w i t h v e r a t r y l a l c o h o l a s the r e d u c i n g s u b s t r a t e , the normal c a t a l y t i c c y c l e i s completed v i a two s i n g l e e l e c t r o n s t e p s (40,46) ( F i g . 2 ) . I n c o n t r a s t to L i P I f o r m a t i o n , the r a t e o f c o n v e r s i o n o f L i P I to L i P I I ( k ) and L i P I I to the n a t i v e enzyme ( k ) a r e s t r o n g l y dependent on pH w i t h optimum a c t i v i t y a t low pH. A p p a r e n t l y the pH dependence o f k and k , r a t h e r than o f k , d i c t a t e the o v e r a l l pH dependence o f the enzyme (46). 2

3

2

3


Manganese P e r o x i d a s e C a t a l y t i c C y c l e The o x i d a t i o n o f phenols and o t h e r o r g a n i c s u b s t r a t e s by MnP i s dependent on M n l l (23,30). A p p a r e n t l y the enzyme f i r s t o x i d i z e s M n l l to M n l l l , and M n l l l s u b s e q u e n t l y o x i d i z e s the o r g a n i c s u b s t r a t e s (30,31,47). As shown i n F i g u r e 3, a d d i t i o n o f one e q u i v a l e n t o f M n l l r a p i d l y reduces MnP compound I to compound I I ( 4 1 ) . A second e q u i v a l e n t o f M n l l reduces MnP compound I I to the n a t i v e f e r r i c enzyme. S i m i l a r l y , MnP compound I i s r e d u c i b l e by p h e n o l i c s u b s t r a t e s , a l b e i t a t a s l o w e r r a t e . However, p h e n o l i c s u b s t r a t e s a r e n o t a b l e t o reduce MnP compound I I e f f i c i e n t l y ( 4 1 ) . Thus the enzyme i s unable to complete i t s c a t a l y t i c c y c l e e f f i c i e n t l y I n the absence o f M n l l . T h i s would seem t o e x p l a i n the a b s o l u t e M n l l r e q u i r e m e n t f o r c a t a l y tic activity. I n the c o n v e r s i o n o f MnP compound I to compound I I , the p o r p h y r i n π-cation i s reduced back to a normal p o r p h y r i n . This suggests t h a t the p o r p h y r i n r a d i c a l i s exposed i n a p e r i p h e r a l s i t e as r e c e n t l y suggested f o r HRP (48) and t h a t t h i s s i t e may be a v a i l a b l e t o o r g a n i c s u b s t r a t e s and to M n l l . I n c o n t r a s t , the FelV^O c e n t e r o f MnP compound I I may be p a r t i a l l y b u r l e d and o n l y a v a i l a b l e to M n l l i o n s . Reactions Catalyzed

by L i g n i n P e r o x i d a s e

L i g n i n p e r o x i d a s e c a t a l y z e s the H 0 - d e p e n d e n t o x i d a t i o n o f a wide v a r i e t y o f n o n p h e n o l i c l i g n i n model compounds to y i e l d numerous p r o d u c t s ( F i g s . 4 and 5 ) . These r e a c t i o n s i n c l u d e b u t a r e n o t l i m i t e d to ( a ) b e n z y l i c a l c o h o l o x i d a t i o n s , (b) C -C3 bond c l e a v a g e , (c) α-methylene h y d r o x y l a t i o n , ( d ) 3 - a r y l e t h e r bond c l e a v a g e and d e m e t h y l a t l o n , ( e ) rearrangements, and ( f ) r i n g - o p e n i n g r e a c t i o n s (24-27,49-51). A l l o f these r e a c t i o n s a r e c o n s i s t e n t w i t h a mechan ism i n v o l v i n g the i n i t i a l o n e - e l e c t r o n o x i d a t i o n o f the s u b s t r a t e by the o x i d i z e d enzyme I n t e r m e d i a t e s L i P I and L i P I I to form an a r y l c a t i o n r a d i c a l f o l l o w e d by a s e r i e s o f nonenzymatic r e a c t i o n s to y i e l d the f i n a l p r o d u c t s (28,52-54). T h i s i s i l l u s t r a t e d i n F i g u r e 5 f o r the o x i d a t i o n o f a 3-1 d i a r y l p r o p a n e d i m e r i c model compound ( 5 4 ) . I n t h i s pathway the o x i d i z e d enzyme i n t u r n o x i d i z e s the d i a r y l propane to form an a r y l c a t i o n r a d i c a l . D i r e c t EPR e v i d e n c e f o r f o r m a t i o n o f a r y l c a t i o n r a d i c a l s by L i P has been p r e s e n t e d ( 5 3 ) . The u n s t a b l e a r y l c a t i o n r a d i c a l undergoes C -C3 c l e a v a g e to form the benzaldehyde (2) and a C C b e n z y l i c r a d i c a l i n t e r m e d i a t e . EPR e v i dence f o r such c a r b o n - c e n t e r e d r a d i c a l i n t e r m e d i a t e s i n L i P o x i d a t i o n has a l s o been p r e s e n t e d ( 5 5 ) . The b e n z y l i c r a d i c a l i n t e r m e d i a t e i s a t t a c k e d p r e f e r e n t i a l l y by 0 under a e r o b i c c o n d i t i o n s and the r e s u l t i n g hydroperoxy r a d i c a l would decompose to form the p h e n y l g l y c o l (3) 2

2

a

a

6

2

2


9.

GOLD E T AL.


H 0 2

H 0

2

2

Compound I Fem

F e I 2 = OtPt]


A

H

Compound Π

Δ

'

Fe ΠΖ = Ο s* Excess H 0 f

2

2

Compound ΙΠ T

Fem 0 Figure 2.

2

C a t a l y t i c cycle of l i g n i n

H 0 2

2

peroxidase.

H 0 2

Compound ΠΙ FelH 0 ~ 2

Figure 3.

C a t a l y t i c cycle of manganese peroxidase.


133




GOLD ET AL.

135



9.

Figure 5.

Mechanism of C -C^ a

cleavage by l i g n i n peroxidase.

( R e p r i n t e d w i t h p e r m i s s i o n from r e f .

54.

Copyright

1986

Academic.)


136


and phenylketol (4) f i n a l products. In the absence of 0 , however, the C C benzylic radical Is oxidized by the enzyme to the corres ponding carbonlum Ion which Is subsequently attacked by H 0 y i e l d i n g the phenylglycol (3). This pathway Is consistent with 0 and H 0 Incorporation studies (54). Thus, the key reaction of LIP with l i g n i n model compounds Is a one-electron oxidation of the substrate to an a r y l cation radical and this i s p a r t i a l l y dependent on the oxidation potential of the aromatic ring. Strong electron withdrawing groups such as benzylic carbonyls suppress the formation of a r y l cation r a d i c a l s (56) while electron donating alkoxy groups tend to activate a r y l cation r a d i c a l formation (51). Once the a r y l cation radical i s formed, In most cases i t can diffuse away from the enzyme active s i t e , where I t can undergo 0 -0β sidechaln cleavage as shown i n Figure 5, or react with H 0, 0 or other r a d i c a l s to y i e l d the other oxidized, hydroxylated, β-ether-cleaved, or ring-opened products seen i n Figure 4. The r a t i o n a l design of substrates has allowed us to study sidechaln cleavage and rearrangement as well as ring-opening reactions i n greater d e t a i l (50,51,57). The 3-ether substructure (12) ( F i g . 4) has no alkoxy groups on r i n g C, one alkoxy group on ring A, and three alkoxy groups on ring B. Since a t l e a s t two r i n g alkoxy groups are usually required to form a r a d i c a l cation, only ring Β w i l l be oxidized. Formation of a r a d i c a l cation on ring Β results i n Its subsequent attack by H 0 or the Ύ or α sidechaln hydroxyle followed by coupling with 0 to y i e l d several possible c y c l i c peroxide Intermediates (49,50). The unstable c y c l i c peroxides undergo a variety of cleavage reactions to y i e l d the f i n a l products 13 through 19 ( F i g . 4) (50). The c y c l i c carbonates 14 and 15 were o r i g i n a l l y Isolated by Higuchl's group (11,49,58). Oxidative aromatic ring cleavage had heretofore been thought to be s o l e l y catalyzed by dioxygenases; however, in the LiP-catalyzed reaction, ring cleavage i s i n i t i a t e d by a one-electron oxidation. 2

6

2

2

1 8

1 8


2

2

α

2

2

2

2

Reactions Catalyzed by Manganese Peroxidase MnP was o r i g i n a l l y characterized as a manganese-dependent l a c t a t e activated peroxidase which could oxidize a variety of phenols and dyes (23). Later i t was reported that the enzyme could readily oxidize Mnll to M n l l l (30,31,47) and that α-hydroxy acids such as lactate activate the system, probably by chelating M n l l l to form stable complexes with a high redox potential (41,47). Recently, we showed that the enzyme could not readily complete i t s c a t a l y t i c cycle In the absence of Mnll (41) explaining MnP*s absolute requirement for Mnll. At low pH the ΜηΙΙΙ/ΜηΙΙ oxidation reduction potential i s 1.5 volts and exogenous M n l l l i s capable of oxidizing the phenols and amines oxidized by the enzyme system (30,31,41,47). A l l of these results indicate that this enzyme system u t i l i z e s f r e e l y d i f f u s i b l e ΜηΙΙ/ΜηΙΙΙ as an obligatory redox couple to oxidize the terminal phenolic substrate, l i g n i n . As shown i n Figure 1, about 10-15% of the phenolic groups In l i g n i n are free. Presumably, the M n l l l can diffuse Into the polymeric matrix and oxidize the polymeric free phenolic groups. The MnP-catalyzed oxidation of a free phenolic 3-1 l i g n i n substructure i s shown i n Figure 6 (Warilshi et a l . , i n




GOLD ET AL.


138


preparation). The i n i t i a l reaction i s a one-electron oxidation of the phenol to form a phenoxy r a d i c a l intermediate. Subsequently, a l k y l phenyl cleavage of the r a d i c a l intermediate would y i e l d products 3 through 5, dehydrogenation would y i e l d the ketone (2) and f i n a l l y , C -C^ would y i e l d the products 6 through 8. With this substrate, r a d i c a l coupling i s inhibited by the presence of a methoxy group a t the 5 position on ring A. a

Conclusions The white r o t basidiomycetous fungus P. chrysosporium produces two e x t r a c e l l u l a r nonspecific peroxidases which catalyze the oxidative degradation of l i g n i n . Both of these enzymes are oxidized by H 0 to form the oxidized intermediate compound I. Depolymerization i s i n i t i a t e d by the one-electron oxidation of the substrate either d i r e c t l y or through the redox mediation of Mn, leading to the formation of substrate free r a d i c a l s . The free r a d i c a l intermediates in turn undergo further reactions, dependent on their structure, ultimately y i e l d i n g the d i v e r s i t y of f i n a l products observed.


2

2

Acknowledgmen ts Work i n MHG's laboratory was supported by grants DMB 8607279 from the NSF and DE-FG06-87ER13715 from the USDOE. Literature Cited 1. 2. 3.

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Extracellular Peroxidases Involved in Lignin Degradation by the White

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