Microbial Degradation of Tannins and Related Compounds - ACS

Chapter 40 Microbial Degradation of Tannins and Related Compounds

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A. M. Deschamps Laboratoire de Microbiologie Alimentaire et de Biotechnologie, Université de Bordeaux I, Avenue des Facultés, 33405 Talence, France

While tannins are usually described as antagonists of numerous microorganisms and being recalcitrant to biodegradation, they can nevertheless be degraded by a large variety of microorganisms. Because of their labile galloyl ester structures, hydrolysable tannins are more readily degraded than condensed tannins. This chapter reviews the limited progress made in understanding the potentially useful processes of the biodegradation of hydrolysable and condensed tannins. T a n n i n s are water-soluble phenolic c o m p o u n d s w h i c h are u s u a l l y e x t r a c t e d f r o m p l a n t m a t e r i a l by h o t water. A f t e r l i g n i n s , they are t h e second most a b u n d a n t group o f plant phenolics. T h e i r t a n n i n g p r o p e r t y is due t o t h e i r c a p a c i t y t o combine w i t h proteins. However, they c a n also c o m p l e x w i t h other p o l y m e r s such as alkaloids, cellulose, a n d p e c t i n s . T a n n i n s are u s u a l l y concentrated i n b a r k s , galls o r leaves o f w o o d y plants (1). T a n n i n s are classified i n t o two different groups, hydroxyzable o r condensed, d e p e n d i n g o n t h e s t r u c t u r e o f the p o l y m e r (2). H y d r o l y z a b l e t a n n i n s are c o m p o s e d o f esters o f g a l l i c a c i d (gallotannins) a n d / o r ellagic a c i d (ellagitannins) w i t h a sugar core, p r e d o m i n a n t l y glucose (see G r o s s , t h i s v o l u m e ) . Some o f the most c o m m o n s t r u c t u r e s are d i g a l l o y l 3,6 glucose or t r i g a l l o y l 1,3,6 glucose ( F i g . 1); such structures have been discussed i n detailed review papers b y H a s l a m (1) a n d M e t c h e a n d G i r a r d i n (2). T h e m a j o r c o m m e r c i a l h y d r o l y s a b l e t a n n i n s are e x t r a c t e d f r o m C h i n e s e g a l l (Rhus semialata), s u m a c h (Rhus coriara), T u r k i s h g a l l (Quercus infectoria), t a r a (Caesalpina spinosa), m y r o b o l a m (Terminalia chebula), a n d chestnut (Castanea sativa (1). T h e second group o f t a n n i n s are the condensed t a n n i n s , o r p o l y m e r i c p r o a n t h o c y a n i d i n s (2). These are composed o f flavonoid u n i t s , a n d are more r e c a l c i t r a n t t o biodégradation t h a n h y d r o l y s a b l e t a n n i n s . O f these, t h e 0097-6156/89/0399-0559$06.00/0 © 1989 American Chemical Society

In Plant Cell Wall Polymers; Lewis, N., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1989.


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i m p o r t a n t c o m m e r c i a l ones are e x t r a c t e d f r o m w a t t l e (Acacia mollissima a n d A. mearnsii), a n d quebracho (Schinopsis lorenizii a n d S. balansae). C o n d e n s e d t a n n i n s are u s u a l l y more a b u n d a n t i n tree b a r k s a n d woods t h a n their h y d r o l y z a b l e counterparts (1). T a n n i n s have l o n g been considered to be i n h i b i t o r s of most m i c r o o r g a n i s m s . F o r e x a m p l e , they are s t r o n g i n h i b i t o r s of Azotobacter and n i t r o g e n - f i x i n g (3), n i t r i f y i n g (4,5) a n d sulfate-reducing b a c t e r i a (6). S o i l b a c t e r i a such as Rhizobium are also often sensitive to t a n n i n s . F o r t h i s reason, t a n n i n s generally r e t a r d the rate of d e c o m p o s i t i o n of vegetable m a t t e r (8) v i a i n h i b i t i o n of b i o d e g r a d a t i v e enzymes of the a t t a c k i n g o r g a n i s m . (9,10). F u n g i , such as Fusarium, Verticillium, Aspergillus, AUernaria (11,12), as w e l l as yeasts (13) can also be i n h i b i t e d b y t a n n i n s . H o w e v e r , other related p l a n t phenolics, such as a n t h o c y a n i n s , flavonoids, catechol, etc., can also i n h i b i t these m i c r o o r g a n i s m s (14). T a n n i n s , w h e n p r o v i d e d i n very h i g h concentrations over extended t i m e periods, can also be t o x i c to higher organisms such as r a t s , r a b b i t s , guinea-pigs (15) a n d m a n ; hence their levels are regulated i n m a n y vegetable foods (16). S o m e a u t h o r s have a t t r i b u t e d the presence of t a n n i n s i n b a r k s or leaves to a defense s y s t e m against predators or decomposing organisms (14,16). Nevertheless, m a n y fungi or b a c t e r i a are quite resistant to t a n n i n s a n d can also degrade t h e m . M i c r o b i a l Degradation of Hydrolyzable Tannins In 1913, K n u d s o n (17) reported t h a t t a n n i c a c i d (the c o m m e r c i a l n a m e of the C h i n e s e g a l l t a n n i n ) c o u l d be degraded by a s t r a i n of Aspergillus niger; p r e v i o u s l y the F r e n c h scientist P o t t e v i n (in 1900) h a d n a m e d t h i s enzyme tannase (10). Since t h e n , most of the progress o n e l u c i d a t i n g the m e c h a n i s m s of h y d r o l y s a b l e t a n n i n biodégradation has o c c u r r e d since 1960. Tannase. T h e enzyme tannase, or t a n n i n - a c y l hydrolase ( E C 3:1:1:20), was described a n d purified f r o m strains of Aspergillus niger by H a s l a m et al. (19) a n d D h a r a n d Bose (20). T h i s enzyme s p l i t s the ester linkage of pendant g a l l o y l groups f r o m glucose i n g a l l o t a n n i n s . S u r p r i s i n g l y , the e n z y m e is not i n d u c e d by t a n n i c a c i d , a n d i n A. niger i t is m o s t l y c e l l wall b o u n d or o n l y s l i g h t l y exocellular (20,21). T h e enzyme's o p t i m a l p H is 4-4.5 a n d its o p t i m a l t e m p e r a t u r e is 3 0 ° C . T a n n a s e has been isolated f r o m m y c e l i a l extracts (22) of other Aspergillus species, as w e l l as f r o m various Pénicillium strains (Table I). T a n n a s e has also been detected i n a yeast c u l t u r e , a l t h o u g h its enzyme h a d different o p t i m a , i.e., the o p t i m a l p H was 6 a n d the t e m p e r a t u r e was 4 0 ° C (26). In Candida sp., tannase h a d a M W of 250,000 a n d was composed of two s u b - u n i t s of g l y c o p r o t e i n s t r u c t u r e (31); the tannase of Aspergillus was also of h i g h m o l e c u l a r weight (24). T a n n a s e has also been detected i n b a c t e r i a l cultures (29), where its o p t i m u m a c t i v i t y was p H 5.5 w i t h different strains isolated f r o m decayed barks. Degradation of Gallotannins. Different investigations o n tannase revealed t h a t t h i s enzyme was not e q u a l l y efficient o n a l l h y d r o l y z a b l e t a n n i n s . T h i s was p a r t i c u l a r l y true for yeast, whose tannase was effective o n l y o n t a n n i c


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T a b l e I. M i c r o o r g a n i s m s P r o d u c i n g T a n n a s e ( t a n n i n - a c y l hydrolase) FUNGI:


Aspergillus niger. H a s l a m et al. (19); P o u r r a t et al. (21) Aspergillus oryzae: I i b u c h i et al. (23) Aspergillus flavus: A d a c h i et al. (24) Aspergillus japonicus: G a n g a et al. (22) Pénicillium chrysogenum: R a j a k u m a r a n d N a n d y (25) Pénicillium notatum: G a n g a et al. (22) Pénicillium islandicum: G a n g a et al. (22) YEASTS: Candida sp.: A o k i et al. (26) Pichia, several species: J a c o b a n d P i g n a l (27) Debaryomyces hansenii: J a c o b a n d P i g n a l (27) BACTERIA: Achromobacter sp: L e w i s a n d S t a r k e y (28) Bacillus pumilus: D e s c h a m p s et al. (29) Bacillus polymyxa: D e s c h a m p s et al. (29) Corynebacterium sp: D e s c h a m p s et al. (29) Klebsiella planticola: D e s c h a m p s et al. (29) Pseudomonas solanacearum: M u t h u k u m a r a n d M a h a d e v a n (30)

a c i d , but not o n n a t u r a l t a n n i n s such as chestnut, oak, m y r o b o l a n or t a r a (27). F u r t h e r , w h i l e A o k i et al. (26,31) were able t o degrade t a n n i c a c i d u s i n g Rhodotorula rubra, i t was o n l y w e a k l y a c t i v e o n chestnut t a n n i n (32). O n the other h a n d , f u n g a l tannases efficiently degrade h y d r o l y s a b l e t a n n i n s . T h i s has been s h o w n by the d e g r a d a t i o n of a m l a (33) a n d m y r o b o l a n (34) t a n n i n s w i t h enzymes f r o m Aspergillus niger, a n d chestnut t a n n i n s w i t h enzymes f r o m different f u n g i (28). T h i s p r o p e r t y is c u r r e n t l y used i n the d e t o x i f i c a t i o n of tea t a n n i n e x t r a c t s u s i n g a n i n d u s t r i a l l y p r o duced e n z y m e f r o m A. niger. B a c t e r i a l tannase l i t e r a t u r e is l i m i t e d to the i s o l a t i o n of a n Achromobacter capable of d e g r a d i n g g a l l o t a n n i n f r o m Chinese g a l l ( L e w i s a n d S t a r k e y , 1969 (28)) a n d our own papers (29,30). I n 1980 (35), we des c r i b e d a collection of t a n n i c a c i d d e g r a d i n g b a c t e r i a , m o s t l y f r o m Bacillus, Corynebacterium a n d Klebsiella s t r a i n s , w h i c h c o u l d degrade n a t u r a l t a n n i n s such as those f r o m chestnut a n d t a r a . Indeed, because of the s i m ple s t r u c t u r e of the g a l l o t a n n i n i n t a r a species, t h i s represents a p o t e n t i a l source of g a l l i c a c i d (36). T h e d e g r a d a t i o n of m y r o b o l a n t a n n i n was also r e p o r t e d for Pseudomonas solanacearum (30). Degradation of Gallic Acid. G a l l i c a c i d , a n o b l i g a t e i n t e r m e d i a t e i n the d e g r a d a t i o n of g a l l o t a n n i n s , is degraded b y some b a c t e r i a such as Pseudomonas (37). In our l a b o r a t o r y , b o t h Klebsiella pneumoniae (38) a n d K. planticola s t r a i n s grew on t a n n i n s a n d u t i l i z e d gallic a c i d as a c a r b o n source (35). T h e same c a p a c i t y was observed for Citrobacter species where p y r o -


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g a l l o l a c c u m u l a t e d as a m e t a b o l i c end p r o d u c t . K o s h i d a a n d Y a m a d a (39) recently patented this m e t h o d for p y r o g a l l o l p r o d u c t i o n . W h i l e gallic a c i d is p r o b a b l y u t i l i z e d b y f u n g i a n d yeasts as a carb o n source, o n l y a few papers have suggested t h i s p o s s i b i l i t y (25,40,41), i n c l u d i n g one for Aspergillus flavus (42).


Microbial Degradation of Condensed Tannins C o n d e n s e d t a n n i n s were considered to be h i g h l y r e c a l c i t r a n t to biodégrad a t i o n u n t i l B a s a r a b a (3) r e p o r t e d t h a t some b a c t e r i a l isolates c o u l d u t i l i z e w a t t l e t a n n i n as b o t h a c a r b o n a n d energy source. L a t e r , L e w i s a n d S t a r k e y (28) isolated a s t r a i n of Pseudomonas w h i c h degraded c a t e c h i n , a n d s t r a i n s of Aspergillus a n d Pénicillium w h i c h degraded w a t t l e t a n n i n . Fungal Degradation of Condensed Tannins. C h a n d r a et al. (43) first rep o r t e d the i s o l a t i o n of f u n g i , such as Aspergillus fumigatus, A. flavus, A. terreus a n d various Pénicillium sp., w h i c h were capable of d e g r a d i n g t a n n i n s e x t r a c t e d f r o m apple w o o d . These observations were e x t e n d e d b y G r a n t (44), u s i n g a s t r a i n of P. adametzi capable of d e g r a d i n g d i - a n d t r i p r o c y a n i d i n s t r u c t u r e s , as well as (+) catechin a n d a crude t a n n i n e x t r a c t . S o m e u n u s u a l w h i t e - r o t f u n g i , identified as Bispora betulina a n d Isaria sp., were also able to degrade condensed t a n n i n s e x t r a c t e d f r o m Douglas-fir bark (45). Recently, S i v a s w a m y a n d M a h a d e v a n (46) r e p o r t e d the d e g r a d a t i o n of wattle t a n n i n by a s t r a i n of Aspergillus niger. Interestingly, i t also p r o d u c e d tannase a n d c o u l d degrade the g a l l o t a n n i n , m y r o b o l a n . T h e edible puffball Calvatia gigantea can also degrade b o t h h y d r o l y z a b l e (chestn u t ) a n d condensed (wattle) t a n n i n s (47), as well as c a t e c h i n . It has been proposed t h a t this o r g a n i s m c o u l d be used for d e t o x i f i c a t i o n purposes, or for the v a l o r i z a t i o n of h i g h - t a n n i n vegetable residues. Yeasts have been described for the d e g r a d a t i o n of w a t t l e t a n n i n (48). T h i s d e g r a d a t i o n was d e t e r m i n e d by the e s t i m a t i o n of l e u c o a n t h o c y a n i d i n a n d flavan-3-ol groups ( F i g . 2) i n the r e m a i n i n g degraded t a n n i n . A m o n g the s t r a i n s (Candida guilliermondii, C. tropicalis, Torulopsis Candida) isolated a n d s t u d i e d , the simultaneous d e g r a d a t i o n of b o t h s t r u c t u r e s was not observed, suggesting different mechanisms of d e g r a d a t i o n . F o r e x a m p l e , a s t r a i n o f C. guilliermondii degraded the flavan-3-ol s t r u c t u r e s b u t d i d not affect the l e u c o a n t h o c y a n i d i n components. M o s t yeasts were efficient degraders of quebracho t a n n i n s (32) a n d reduced the t a n n i n content of pine a n d g a b o o n w o o d b a r k extracts b y 70 to 8 0 % i n five days. Bacterial Degradation of Condensed Tannins. A l t h o u g h B a s a r a b a (5) p r o posed t h a t b a c t e r i a c o u l d degrade condensed (wattle) t a n n i n , t h i s t o p i c has o n l y been investigated i n our l a b o r a t o r y i n C o m p i e g n e . In these studies, our objective was to c o n t r o l the rate of biodégradation of t a n n i n - r i c h b a r k s , such as those f r o m pine a n d g a b o o n - w o o d (Acoumea kleneana). Consequently, we succeeded i n i s o l a t i n g , b y c u l t u r e e n r i c h m e n t , b a c t e r i a capable of d e g r a d i n g a n d u t i l i z i n g these b a r k s (49), as w e l l as quebracho (Schinopsis lorentzii) a n d wattle (Acacia mollissima) t a n n i n s . A collection of various genera a n d species was identified i n these studies (50), w i t h the genera


DESCHAMPS

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40.

F i g u r e 2. (a) L e u c o a n t h o c y a n i d i n a n d (b) R ' a n d R " = H or O H .

flavan-3-ol

s t r u c t u r e s , where R ,


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Bacillus, Klebsiella, Corny bacterium, a n d Pseudomonas b e i n g the most frequently observed. T h e c a p a c i t y of these b a c t e r i a to degrade t a n n i n s , a n d detoxify b a r k chips or b a r k s e x t r a c t s , was further d e m o n s t r a t e d w i t h pine (Pinus maritima) (51), oak (Quercus pedonculata) and gaboon wood (Aucoumea kleneana) b a r k s (52). T h e d e g r a d a t i o n of quebracho a n d w a t t l e t a n n i n s was also confirmed i n pure cultures (53). Microbial Degradation of Catechin. Since (+) catechin is a possible biodégradation p r o d u c t f r o m condensed t a n n i n s , i t s u t i l i z a t i o n a n d b i o c o n version have been extensively e x a m i n e d b y several research groups u s i n g f u n g i , b a c t e r i a a n d yeasts. Fungi. F u n g i - d e g r a d i n g c a t e c h i n have been k n o w n for about twenty years, e.g., Aspergillus niger, A. terreus, A. fumigatus, A. flavus a n d Pénicillium sp. (54) a n d Pénicillium adametzi (44). In the l a t t e r case, the o r g a n i s m grew o n catechin a n d a n t h o c y a n i d i n m o d e l c o m p o u n d s as sole carb o n sources. Interestingly, the pathogenic fungus Endothia parasitica (55) also degraded c a t e c h i n . T o account for its biodégradation, C h a n d r i et al. (54) first suggested t h a t an e x t r a c e l l u l a r enzyme must be i n v o l v e d , f o l l o w i n g w h i c h the enzyme catechin 2,3-dioxygenase was isolated f r o m Chaetomium cupreum (56). T h e molecular weight ( M W ) of t h i s g l y c o p r o t e i n was a p p r o x i m a t e l y 40,000 a n d catechin was cleaved v i a meta-nng fission. Bacteria. M a n y b a c t e r i a degrade catechin a n d use it as a c a r b o n source, as s h o w n first by L e w i s a n d S t a r k e y (28). In 1982 M u t h u k u m a r et al. isolated several strains of Rhizobium a n d Bradyrhizobium (57), i n c l u d i n g B. japonicum w h i c h degraded catechin. T h i s last species p r o d u c e d the same enzyme as C. cupreum ( W a h e e t a a n d M a h a d e v a n , p e r s o n a l c o m m u n i c a t i o n ) . W e also d e m o n s t r a t e d t h a t c e r t a i n t a n n i c - a c i d d e g r a d i n g b a c t e r i a can also degrade catechin (35). R e c e n t l y , B a o m i n a t h a n a n d M a hadevan showed t h a t catechin-degrading m a c h i n e r y was p l a s m i d borne i n Pseudomonas solanacearum (58), w h i c h also produces a catechin oxidase. Yeasts. A n interesting paper p u b l i s h e d i n 1984 (59) c l a i m e d t h a t r a t caecal m i c r o f l o r a degraded c a t e c h i n . T o our knowledge no paper has dealt w i t h yeasts, other t h a n t h a t some yeasts d e g r a d i n g w a t t l e of quebracho t a n n i n s were able to grow weakly w i t h catechin as a sole c a r b o n source (32). Concluding Remarks T h i s review of l i t e r a t u r e on t a n n i n d e g r a d a t i o n shows t h a t our knowledge of t h i s t o p i c is o n l y very slowly i m p r o v i n g . O n l y a h a n d f u l of laboratories are c u r r e n t l y i n v o l v e d i n this area. O f these, the I n d i a n laboratories have m a d e several i n t e r e s t i n g investigations recently, p r e s u m a b l y because they are very active i n leather manufacture a n d need to c o n t r o l the t o x i c i t y of their tannery effluents. Some m i c r o o r g a n i s m s d e g r a d i n g condensed t a n n i n s have been isolated and described, but no reports on the m e c h a n i s m of the d e p o l y m e r i z a t i o n process, or the enzymes involved i n biodégradation, have a p p e a r e d . It must be stressed t h a t condensed t a n n i n d e g r a d a t i o n m a y be associated w i t h other



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detoxification mechanisms, other than those operative for catechin. This assertion is made since many strains which grow on condensed tannins do not grow on catechin. This is unusual since this compound is often viewed as an intermediate of biodégradation. Consequently, catechin degradation should not be confused with condensed tannin degradation. More studies are needed, if we are to understand and elucidate the mechanism of the degradation of condensed tannins. Currently, there is insufficient data available for comparison of this degradation process to that of other polyphenols, such as lignin. Further, while the degradation mechanisms of tannic and gallic acids are quite well understood for bacteria and fungi, few commercial applications have yet resulted, e.g., in the production of the enzyme tannase or the bioconversion of gallic acid (or tannins) to pyrogallol (60). In the case of the condensed tannins, however, their biodégradation has been much less thoroughly studied. Such studies are important since control and detoxification of tannins will continue to find application in the food industry (61), as well as in biotechnological processes using barks as lignocellulosic substrates (62). For these reasons, the isolation and identification of tannindegrading enzymes, and the determination of their mechanism of action, are of great importance. Literature Cited 1. Haslam, E . In Biochemistry of Plant Phenolics; Plenum Press: New York, 1979, 475-523. 2. Metche, M.; Girardin, M. In Les PolymeresVegetaux; Monties, B., Ed.; Gauthiers Villars: Paris, 1980. 3. Basabara, J. Can. J. Microbiol. 1966, 12, 787-794. 4. Rice, E. L.; Pancholy, S. K.; Am. J. Bot. 1973, 60, 691-702. 5. Basabara, J. Plant Soil 1964, 21, 8-16. 6. Booth, G . H. J. Appl. Bacteriol. 1960, 23, 125-129. 7. Muthukumar, G.; Mahadevan, A. Leather Sci. 1983, 30, 263-269. 8. Benoit, R. E.; Starkey, R. L. Soil Sci. 1968, 105, 203-208. 9. Goldstein, J. L.; Swain, T . Phytochem. 1965, 4, 185-192. 10. Benoit, R. E.; Starkey, R. L. Soil Sci. 1968, 105, 203-208. 11. Lewis, J. Α.; Papavizas, G . C. Can. J. Microbiol. 1967, 13, 1655-1661. 12. Mahadevan, Α.; Muthukumar, G. Hydrobiol. 1980, 72, 73-79. 13. Jacob, F. H.; Pignal, M . C. Mycopathol. Mycol. Appl. 1972, 48, 121142. 14. Mahadevan, A. J. Sci. Indian Res. 1974, 33, 131-138. 15. Cameron, G. R.; Milton, R. F.; Allen, J. W. Lancet 1943, 14, 179-186. 16. MacLeod, M . N. Nutr. Abs. Rev. 1974, 44, 803-815. 17. Knudson, L. J. Biol. Chem. 1913, 14, 159-184. 18. Pottevin, H. Compt. rend. 1900, 131, 1215-1217. 19. Haslam, E.; Haworth, R. D.; Jones, K.; Rogers, H. J . J. Chem. Soc. 1961, 1821-1835. 20. Dhar, S. C.; Bose, S. M . Leather Sci. 1964, 11, 27-38.



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