FEMS Microbiology Reviews Volume 15 issue 2-3 1994 [doi 10.1111%2Fj.1574-6976.1994.tb00137.x] Jan Roelof van der Meer -- Genetic adaptation of bacte.pdf

8/11/2019 FEMS Microbiology Reviews Volume 15 issue 2-3 1994 [doi 10.1111%2Fj.1574-6976.1994.tb00137.x] Jan Roelof v

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FEMS Microbiology Reviews 15 (1994) 239-249

g' 1994 Federation of European Microbiological Societies 0168-6445/94/ 15.0t)

Published by Elsevier

239

FEMSRE 00433

G e n e t i c a d a p t a t io n o f b a c t er ia t o c h l o r in a t e d

a r o m a t i c c o m p o u n d s

J a n R o e l o f v a n d e r M e e r

EAWAG, Ueberlandstr. 133, Ctt-8600 Diibendo( Switzerland

Abstracc Genetic mechanisms in bacteria provide a continuous source of aherations in DNA sequences that may lead to

favourable adaptations. Bacteria that use chlorinated aromatics as sole carbon and energy sources show evidence of these different

genetic alterations. The distinct effects of single base-pair mutations on adaptation of bacterial strains (e.g. by changing the

substrate specificity of a key metabolic enzyme or regulator protein) have been demonstrated in various studies. In addition to

these small sequence modifications, intermolecular or intercellular gene exchange mechanisms can result in new strains with

altered metabolic capabilities. The details of these evolutionary processes with respect to the m etabolism of chlorobenzene s and

chlorocatechols are reviewed in this manuscript.

Key words:

Adaptation; Pseudomonads; Chlorinated aromatic compounds: Evolution

I n t r o d u c t i o n

O v e r t h e p a s t f e w d e c a d e s , t h e l a r g e s ca l e

i n d u s t r i a l p r o d u c t i o n a n d e x t e n s i v e u s e o f s y n -

t h e t i c c h e m i c a l s i n a l l l e v e l s o f s o c i e t y h a v e l e d t o

a w i d e d i s t ri b u t io n o f h a r m f u l c o m p o u n d s in t h e

e n v i r o n m e n t . I n a l m o s t a ny c o m p a r t m e n t o f o u r

e n v i r o n m e n t e . g . s o il , a i r , w a t e r , a n d b i o t a ) ,

t r a c e s o f s y n t h e ti c o r g a n i c c o m p o u n d s c a n b e

d e t e c t e d . A t m a n y w a s t e d i s p o s a l s it e s o r o t h e r

p o i n t s o u r c e s o f c o n t a m i n a t i o n , c o n c e n t r a t i o n s o f

t h e s e c h e m i c a l s m a y b e s o g r e a t t h a t d i r e c t t o x i-

c o l o g i c a l r i s k s a r e e n c o u n t e r e d .

M i c r o o r g a n i s m s p l a y a c e n t r a l r o l e i n t h e

d e g r a d a t i o n o f o r g a n ic c o m p o u n d s a n d t h e r e f o r e

a r e v e r y i m p o r t a n t f o r t h e m i n e r a l i z a t i o n o r

* Cor res pond ing author . Tel.: ( + 41-1 )823 5438; Fax: (+ 41-1 )

823 5547

d e t o x i f i c a t i o n o f to x i c o r g a n i c c h e m i c a l s . U n f o r -

t u n a t e l y , n o t a l l o r g a n i c c o m p o u n d s a r c e q u a l l y

w e l l b i o d e g r a d a b l e , a n d , i n s o m e c a s e s , e n v i r o n -

m e n t a l c o n d i t io n s m a y b e u n f a v o u r a b l e f o r m i -

c r o b i a l a c t i vi ty . I f t h e m o l e c u l a r s t r u c t u r e o f a

c o m p o u n d is n o t c o m m o n l y e n c o u n t e r e d in n a-

t u r e , m i c r o o r g a n i s m s m a y n o t h a v e t he n e c e s s a r y

d e g r a d a t i v e e n z y m e s y st e m s . T h e p r e s e n c e o f

s u b s t i t u e n t s , s u c h a s h a l o g e n a t o m s , n i t r o - o r

s u l f it e g r o u p s , o n o t h e r w i s e e a s i l y d e g r a d a b l e

c o m p o u n d s m a y m a k e t h e c o m p o u n d l es s a c c e ss i -

b l e f o r b i o d e g r a d a t i o n a n d t h u s m o r e p e r s i s t e n t

i n t h e e n v i r o n me n t [ 1 , 2 ] .

I t h a s b e e n s h o w n t h a t m i c r o b i a l p o p u l a t i o n s

m a y a d a p t t o u s e p re v i o u s l y p e r s i s t e n t c o m -

p o u n d s a s n ov e l c a r b o n a n d e n e r g y s o u r c e s [ 3 - 5] .

S u c h a n a d a p t a t i o n m a y b e c a u s e d b y t h e s e le c -

t io n o f m u t a n t s t r a in s w h i ch h a v e a c q u i r e d n o v e l

m e t a b o l i c a c t i v i t i e s o r a l t e r e d e n z y m a t i c s p e c i f i c i -

t ie s . H e r e 1 d i s c u s s s o m e o f th e g e n e t i c m e c h a -

SSDI 0 1 6 8 - 6 4 4 5 ( 9 4 ) 0 0 0 3 5 - W


2/11

24(I

n i s m s w h i c h m a y h a v e r e s u l t e d i n t h e f o r m a t i o n

o f t h e m e t a b o l i c p a t h w a y o f c h l o r i n a t e d b e n z e n e

d e g r a d a t i o n i n p s e u d o m o n a d s .

G e n e t i c m e c h a n i s m s f o r a d a p t a t i o n

A w i d e v a r i e t y o f p r o c e s s e s e x i s t t h a t c a u s e

c h a n g e s i n e x i s t i n g g e n e t i c m a t e r i a l a n d r e s u l t i n

a l t e r e d m e t a b o l i c f u n c t io n s . T h e d e t a i ls o f t h e

d i f f e r e n t g e n e t i c m e c h a n i s m s i n a d a p t a t i o n t o

x e n o b i o t i c c o m p o u n d s h a v e r e c e n tl y b e e n r e -

v i e w e d e l s e w h e r e [ 6 , 7 ] . W h e n c o n s i d e r i n g t h e d i f -

f e r e n t g e n e t i c m e c h a n i s m s i n v o l v e d i n e v o l u t i o n

a n d a l t e r a t io n s o f D N A s e q u e n c e s , a d i st i nc t io n

s h o u l d b e m a d e b e t w e e n v e r t i c a l a n d h o r i z o n t a l

e v o l u t i o n a r y p r o c e s s e s [ 8 ] . V e r t i c a l p r o c e s s e s a r e

t h o s e w h i c h l e a d t o a d i v e r g e n c e i n D N A s e -

q u e n c e i n d a u g h t e r c e l l s , d u e t o t h e a c c u m u l a t i o n

o f m u t a t i o n s . T h e s e m u t a t i o n s c a n b e s i n gl e

b a s e - p a i r c h a n g e s o r t h o s e l e a d i n g t o l a r g e r s e -

q u e n c e c h a n g e s , e . g . d e l e t i o n s a n d d u p l i c a t i o n s .

T h e e f f e c t s o f p o in t m u t a t i o n s o n e n z y m e s p e c i-

f i ci ty o r o n e f f e c t o r r e c o g n i t i o n b y r e g u l a t o r p r o -

t e i n s h a v e b e e n w e l l e s t a b l i s h e d [ 9 - 1 2 ] , a n d i t h a s

b e c o m e c l e a r t h a t t h e s e p r o c e s s e s c a n h a v e d i r e c t

c o n s e q u e n c e s f o r t h e a d a p t a t i o n o f s t r ai n s to

x e n o b i o t i c c o m p o u n d s . O t h e r p o s s i b l e p r o c e s s e s

o f s e q u e n c e d i v e r g e n c e , e .g . s li p p e d s t r a n d m i s -

p a i r i n g , c a n l e a d t o m o r e e x t e n s i v e s e q u e n c e

c h a n g e s a n d m a y b e a g e n e r a l d r i v i n g f o r c e f o r

t h e d i v e r g e n c e o f g e n e s e q u e n c e s [ 1 3 -1 5 ] . T h e

e f f e c t o f s u c h a p r o c e s s i n m i c r o o r g a n i s m s , h o w -

e v e r , h a s n o t y e t b e e n w e l l i n v e s t i g a t e d .

H o r i z o n t a l p r o c e s s e s a r e t h o s e w h i c h c a u s e a n

e x c h a n g e o f D N A s e q u e n c e s b e tw e e n t h e g e n o m e

o f tw o d i f f e r e n t o r g a n i s m s ( i n t e r c e l lu l a r m o v e -

m e r i t ) , o r b e t w e e n d i f f e r e n t D N A m o l e c u l e s , e . g .

w i t h i n t h e c h r o m o s o m e a n d e x t r a c h r o m o s o m a l

e l e m e n t s i n s i d e o n e o r g a n i s m ( i n t e r m o l e c u l a r

m o v e m e n t ) [8]. H o r i z o n t a l m o v e m e n t o f g e n e t i c

i n f o r m a t i o n m a y b e c a u s e d b y r e c o m b i n a t i o n o r

o t h e r m e c h a n i s m s o f g e n e e x c h a n g e , e .g . c o n j u g a -

t i o n , t r a n s d u c t i o n , o r t r a n s f o r m a t i o n . I t h a s b e -

c o m e v e r y c l e a r t h a t h o r i z o n t a l g e n e e x c h a n g e

p l a y s a n i m p o r t a n t r o le i n th e a d a p t a t i o n o f m i -

c r o o r g a n i s m s t o x e n o b i o t i c c o m p o u n d s [ 6 ] . T h e

l is t o f b a c t e r i a w i t h s e l f - t r a n s m i s s a b l c p l a s m i d s

e n c o d i n g t h e d e g r a d a t i o n o f a r o m a t i c o r to x ic

o r g a n i c c o m p o u n d s i s e x t e n s i v e [ 1 6 ] . A l t h o u g h

m a n y o f th e s e p l a s m i d s h a v e a s i m i la r b a c k b o n e

s t r u c t u r e e n c o d i n g p r o b a b l y r e p l i c a ti o n a n d

t r a n s f e r f u n c t i o n s , t h e y c a r r y d i f f e r e n t c a t a b o l i c

g e n e s [ 1 7 ] . T h i s s t r o n g l y s u g g e s t s t h e e x i s t e n c c o f

p r o c e s s e s b y w h i c h p l a s m i d s c a n a c q u i r e g e n e s o r

g e n e c l u s t e r s a n d s u b s e q u e n t l y d i s s e m i n a t e t h e m

i n a mi c r o b i a l p o p u l a t i o n [ 1 8 , 1 9 ] . Su c h a r e c e n t

e x a m p l e o f h o r i z o n t a l g e n e e x c h a n g e h a s b e e n

t h e d i s c o v e r y o f t r a n s p o s a b l e e l e m e n t s o f d i f f e r-

e n t f a m i l i c s c o n t a i n i n g c a t a b o l i c g e n e s . T h e xyl

a n d

nah

g e n e s a r c l o c a t e d o n T n 3 - t y p e t r a n s -

p o s o n s ,

Tn4561

( 5 6 k b ) [ 2 ( I] a n d

Tn4655

( 5 5 k b )

[ 2 1 ] , r e s p e c t i v e l y . O t h e r e l e m e n t s w h i c h h a v e b e e n

d e s c r i b e d i n c l u d e

Tn5271,

e n c o d i n g 4 - c h l o r o b e n -

z o a t e m e t a b o l i s m [ 2 2 ] , Tn4371, f o r 4 - c h l o r o b i -

p h e n y l m e t a b o l i s m [ 2 3 ] , 1 S 9 3 1 , a s s o c i a t e d w i t h

t h e 2 , 4 , 5 - t r i c h l o r o p h e n o x y a c e t i c a c i d g e n e s [ 24 ],

t h e DEH e l e m e n t , w h i c h c a r r i e s t h e d e h a l o g e -

n a s e g e n e s o f Pseudomonas putida PP3 [25] , and

Tn5280

o f t h e c h l o r o b e n z e n e p l a s m i d p P 5 1 [ 26 ]

( s e e b e lo w ) . S o m e o f t h e s e e l e m e n t s r e s i d e o n t h e

c h r o m o s o m e ( s u c h a s I S 9 3 1 , Tn4371, a n d DEH ,

w h e r e a s t h e o t h e r s w e r e o r i g i n a l l y i s o l a t e d f r o m

p l a s m i d s .

E vol u t i on o f th e m e tab o l i c p a th way for c h l or o -

b e n z e n e d e g r a d a t i o n

S i nc e v e r y f e w b a c t e r i a h a d b e e n d e s c r i b e d

w h i c h w e r e a b l e t o d e g r a d e c h l o r o b e n z e n e s c o m -

p l e te l y , w e c o n s i d e r e d t h e s e c o m p o u n d s s u i ta b l e

s u b s t r a t e s f o r e v o l u t i o n a r y s t u d i e s o f b a c t e r i a l

a d a p t a t i o n . C h a r a c t e r i z a t i o n o f

Pseudomonas

sp .

s t r a i n P 5 1 , c a p a b l e o f d e g r a d i n g 1 , 2 , 4 -t r ic h l o r o -

b e n z e n e , 1 , 2 - d i c h l o r o - a n d 1 , 4 - d i c h l o r o b e n z e n e ,

a l o n g w i t h s t r a i n s i s o l a t e d b y o t h e r s [ 5 , 2 7 - 2 9 ], l e d

t o a r e a s o n a b l y g o o d p i c t u r e o f th e m e t a b o l i c

p a t h w a y f o r c h l o r o b e n z e n e d e g r a d a t i o n a n d o f

t h e d i f f e r e n t g e n e s w h i c h a r e i n v o l v e d i n t h is

p a t h w a y [ 2 6 , 2 9 - 3 1 ] . T h e f i r s t e n z y m e s o f t h e

p a t h w a y , a t h r e e - c o m p o n e n t a r o m a t i c r i n g d i o x y -

g e n a s e a n d a b e n z e n e g ly c ol d e h y d r o g e n a s e , c a t -

a l y z e t h e i n c o r p o r a t i o n o f a d io x y g e n m o l e c u l e

i n t o t h e a r o m a t i c r i n g a n d t h e s u b s e q u e n t d e h y -

d r o g e n a t i o n w h i c h g i v e s r i se t o a c h l o r i n a t e d


3/11


4/11

242

[ 2 6 ,2 9 - 3 1] . T h e u p p e r p a t h w a y g e n e c l u s t e r in

s t r a i n P 5 1 i s f l a n k e d b y t w o i s o - i n s e r t i o n e l e -

m e n t s , ISI06O a n d IS1007. T h i s c o m p l e t e e l e -

m e n t ,

Tn5280,

w a s s h o w n t o b e a f u n c t i o n a l

t r a n s p o s o n , a b l e t o i n s e r t in s in g l e c o p y a n d a t

r a n d o m i n t o t h e g e n o m e [ 2 6 ] .

A s a r e s u l t o f t h e s e a n a l y s e s , it a p p e a r s t h a t

t h e m e t a b o l i c p a t h w a y f o r c h l o r o b e n z e n e d e g r a -

d a t i o n i n s t r a i n P 51 d e v e l o p e d f r o m t w o d i f f e r e n t

g e n e t i c e l e m e n t s . T h e t r a n s p o s a b l e c l c m e n t c o n -

t a i n i n g t h e g e n e s f o r t h e a r o m a t i c r i n g d i o x y g c -

n a s e a n d t h e b e n z e n e g l y c o l d e h y d r o g e n a s e , i . e.

Tn5280,

m a y h a v c o r i g i n a t e d in b a c t e r i a d e g r a d -

i n g t o l u e n e b y d i r e c t d i o x y g e n a t i o n , s u c h a s P .

putida F1 [ 3 2 ] . T h e d i o x y g e n a s e i n t h i s s t r a i n w a s

s h o w n t o h a v e a b r o a d s u b s t r a t e r a n g e , a n d c o u l d

o x i d i z e c h l o r i n a t e d b e n z e n e s t o t h e c o r r e s p o n d -

i n g d ih y d r o d i o l s [ 3 2]. I f s u c h a d i o x y g e n a s e g e n e

c l u s t e r b e c a m e c a p t u r e d b y t w o c o p ie s o f a n

i n s e r t i o n e l e m e n t , i . e . IS1066 a n d IS1007, s u c -

c e s s fu l t r a n s f c r o f t he d i o x y g e n a s e t r a n s p o s o n t o

a c a t a b o l i c p l a s m i d c o n t a i n i n g a c h l o r o c a t e c h o l

o x i d a t i v e o p e r o n , c o u l d p r o v i d e t h e r e s u l t i n g

t r a n s c o n j u g a n t s t r a i n w i t h t h e n e c e s s a r y g e n e t i c

i n f o r m a t i o n t o ca r r y o u t c o m p l e t e c h l o r o b e n z e n e

d e g r a d a t i o n . S t r a i n P 5 1 , t h e n , p r o v i d e s a n i c e

e x a m p l e o f d i f f e r e n t c w ) l u t io n a r y m e c h a n i s m s

w h i c h m a y b c r e q u i r e d f o r th e g e n e r a t i o n o f a

n e w c a t a b o l i c p a t h w a y , i . e . ( i ) r e c o m b i n a t i o n

e v e n t s i n v o l v i n g h o r i z o n t a l g e n e t r a n s f e r , a n d ( i i)

v e r t i c a l e v o l u t i o n o f s p e c i a l i z e d e n z y m e s y s t e m s

f o r n e w ( c h l o r i n a t e d ) s u b s t r a t e s ( s e e b e l o w ) .

C o n v e r g e n c e a n d v a r i a t i o n s i n m e t a b o l i c p a t h -

w a y s f o r c h l o r o- ) a r o m a t i c c o m p o u n d s

I t h a s b e e n e s t a b l i s h e d t h a t m e t a b o l i c p a t h -

w a y s o f a r o m a t i c c o m p o u n d s in b a c t e r i a g e n e r a ll y

f o l l o w s i m i l a r s t r a t e g i e s a n d i n v o l v e a l i m i t e d

n u m b e r o f c e n t r a l s t e p s . P a t h w a y s f o r a e r o b ic

d e g r a d a t i o n o f a r o m a t i c s a p p a r e n t l y c o n v e r g e to

f o r m a r e l a t iv e l y s m a l l n u m b e r o f i n t e r m e d i a t e s

( F i g . 1 ). T h e s e i n t e r m e d i a t e s c a r r y a t le a s t tw o

h y d r o x y l g r o u p s ( i n

ortho

o r

para

p o s i t i o n s ) a n d

c a n c o n t a i n o t h e r s u b s t i tu e n t g r o u p s . T h e y a r c

t h e n c l e a v e d e i t h e r b y in t r a d i o l d i o x y g e n a s e e n -

z y m e s (ortho c l e a v a g e ) o r b y e x t r a d i o l d i o x y g e -

n a s e s

(meta

c l e a v a g e ) . T h e i n t r a d i o l a n d e x t r a -

d i o l d i o x y g e n a s e s a p p e a r t o h a v e n o s i g n i f i c a n t

s i m i l a r i t i e s o n t h e a m i n o a c i d l e v e l , a n d t h e r e f o r e

a r e n o t e v o l u t i o n a r y c l o s e ly r e l a t e d [3 3]. W i t h i n

t h e e x t r a d i o l d i o x y g e n a s e s a n d i n t r a d i o l d i o x y g e -

n a s e s , d i f f e r e n t e n z y m e g r o u p s a l s o e x i s t w i t h

r e l a t iv e l y li tt le s e q u e n c e s i m i la r i ty . T h e a r c h e t y p e

e x t r a d i o l d i o x y g e n a s e , c a t e c h o l 2 , 3 - d i o x y g e n a s e

( e n c o d e d b y t h e x y l E ,

nahH or dmpB

g e n e s )

( F ig . I B ) , d o e s n o t s h o w s i g n i f ic a n t s e q u e n c e

s i m i l a r it y w i t h t h e e x t r a d io l e n z y m e p r o t o c a t e -

c h u a t e 4 , 5 - d i o x y g e n a s e [ 3 4 ] . O f t h e i n t r a d i o l

d i o x y g e n as e s , th r e e s u b g r o u p s h a v e b e e n d e -

s c r i b e d : c a t e c h o l 1 , 2 - d i o x y g e n a se ( e n c o d e d b y

catA o f Acinetobacter calcoaceticus or P. putida )

[1 4], p r o t o c a t e c h u a t e 3 , 4 - d i o x y g e n a s e ( e n c o d e d b y

t h e pcaHG g e n e s o f e . g . P , putida, P. cepacia, A.

calcoaceticus)

[ 35 - 3 7] , a n d c h l o r o c a t e c h o l 1 , 2 -d i -

o x y g e n a s e ( e n c o d e d b y

tcbC

o f

Pseudomonas

sp .

s t rain P51 [30], tfdC of Alcaligenes eutrophus

[38,39], or ch'A of P . putida p A C 2 7 [ 4 0 ] , a n d

d e s c r i b e d f o r

Pseudomonas

sp. B13 [41]).

A m o n g t h e e n z y m e s w h ic h c a t a l y z e t h e i n it ia l

s t e p s i n a r o m a t i c d e g r a d a t i o n p a t h w a y s , d i f f e r e n t

c l a s s e s a r e f o u n d w i t h e x t e n s i v e h o m o l o g y to e a c h

o t h e r a n d t o o t h e r e n z y m e s o f t h e c e n t r a l p a t h -

w a y s ( F i g . I ) , s u g g e s t i n g s i m i l a r e v o l u t i o n a r y

s t r a t e g i e s . T h e m o s t i m p o r t a n t c l a s s o f t h e s e e n -

z y m e s i s p r o b a b l y t h a t o f t h e a r o m a t i c r i n g d i o x y -

g e n a s e s , w h i c h c a t a l y z e i n s e r t i o n i n t o t h e a r o -

m a t i c r i n g o f t w o h y d r o x y l g r o u p s d e r i v e d f r o m

m o l e c u l a r o x y g e n a n d c o f a c t o r s s u c h a s N A D H

( r e c e n t l y r e v i e w e d in r e f e r e n c e s [4 2 , 43 ] ). I t c u r -

r e n t l y a p p e a r s t h a t a l l o f th e s e d i o x y g e n a s e s a r e

m u l t i - c o m p o n e n t e n z y m e s w i t h th r e e o r f o u r d if -

f e r e n t p r o t e i n s u b u n i t s . T h e s e p r o t e i n s c o m p r i s e

a s h o r t e l e c t r o n t r a n s f e r c h a i n , b y w h i c h e l e c t r o n s

a r e t r a n s f e r r e d f r o m N A D H , v i a a r e d u c t a s e a n d

a f e r r e d o x i n , t o t h e t e r m i n a l o x i d a s e . T h e r e d u c -

t a se a n d t h e f e r r e d o x i n m a y b e c o m b i n e d a s t w o

d o m a i n s o f o n e p r o t e i n m o l e c u l e , a s is t h e c a s e

f o r t h e t o l u a t e a n d b e n z o a t e d i o x y g e n a s e s [ 1 3 , 4 4 ] .

I n s o m e c a s e s , t h e d i f f e r e n t p r o t e i n s u b u n i t s o f

t h e a r o m a t i c r i n g d i o x y g e n a s e s s h a r e s i g n i fi c a n t

a m i n o a c i d s e q u e n c e h o m o l o g y , e . g . t h e t w o s u b -

u n i ts w h i c h m a k e u p t h e t e r m i n a l o x i d a s e o f t h e

t o l u a t c d i o x y g e n a s e a n d t h o s e o f t h e n a p h t h a -

l e n e , t o l u e n e o r b i p h e n y l d i o x y g e n a s e [ 4 4 , 4 5 ] .


5/11

43

M a n y o t h e r a r o m a t i c r i n g d i o x y g e n a s e s h a v e r i o t

y e t b e e n c h a r a c t e r i z e d o n t h e D N A s e q u e n c e

l e ve l , a n d c o m p a r i s o n c a n o n l y b e m a d e o n t h e

b a s i s o f b i o c h e m i c a l i n f o r m a t i o n [ 4 3] .

A n o t h e r c l a s s o f e n z y m e a c t i v i t i e s c a t a l y z i n g

i n i t i a l s t e p s i n a r o m a t i c m e t a b o l i s m a r e t h e

m o n o o x y g e n a s e s o r h yd r o x y la s e s . T h e s e c a t a l y z e

t h e i n c o r p o r a t i o n o f a s in g l e h y d ro x y l g r o u p o n

t h e a r o m a t i c r i n g o r o x i d i z e a l k y l s i d e c h a i n s .

S e v e r a l d i f f e r e n t e n z y m e g r o u p s a r e f o u n d w h i c h

a r e n o t s i g n i fi c a n t l y r e l a t e d o n a m i n o a c i d s e -

q u e n c e l e v e l . S i n g l e c o m p o n e n t a r o m a t i c r i n g

f l a v o p r o t e i n h y d r o x y l a s e s a r e e x e m p l i f i e d b y p -

h y d r o x y b e n z o a t e h y d r o x y la s e , w i th a m o n o m e r

s i z e o f 4 5 k D a [ 46 ]. A n o v e r a l l a m i n o a c i d s e -

q u e n c e i d e n ti ty o f 2 5 w a s f o u n d b e t w e e n p - h y -

d r o x y b e n z o a t e h y d r o x y l a s e a n d s a li c y la t e h y d r o x -

y la s e ( e n c o d e d b y t h e N A H p l a sm i d g e n e

n a h G

[4 7], w h e r e a s 2 , 4 - d i c h l o r o p h e n o l h y d r o x y l a s e (e n -

c o d e d b y t h e g e n e t f d B o f p l a s m i d p J P 4 ) [ 38 ] a n d

p h e n o l h y d r o x yl a se ( e n c o d e d b y p h e A [48] are

s u b s t a n t i a l l y l a r g e r , a n d o n l y s h a r e s i g n i f i c a n t

s e q u e n c e s i m i la r i ty i n t w o r e g i o n s , o n e o f w h i c h

m a y b e i n v o l v e d in F A D b i n d in g . T h e 2 , 4 - d i c h lo -

r o p h e n o x y a c e t i c ac id m o n o o x y g e n a s e ( e n c o d e d b y

t f dA o n p l a s m i d p J P 4 ) i s n o t r e l a t e d t o t h e s e

s i ng l e c o m p o n e n t m o n o o x y g e n a s e s [4 3]. R e c e n t l y

i t w a s r e p o r t e d , h o w e v e r , t h a t t h e e n z y m e i s a

f e r r o u s - i o n - a n d c ~ - k e t o g l u t a r a t e - d e p e n d e n t d i -

o x y g e n a s e , r a t h e r t h a n a m o n o o x y g e n a s e [4 9].

M u l t i c o m p o n e n t a r o m a t i c ri n g m o n o o x y g e n a s e s

a r e a l so f o u n d , e . g . p h e n o l h y x d r o x y l a s e f r o m

Pseudornonas C F 6 0 0 ( e n c o d e d b y t h e d m p -

K L M N O P g e n e s ) [ 5 0 ] , a n d t o l u e n e 4 - m o n o -

o x y g e n a s e f r o m P. mendoc ina K R 1 ( e n c o d e d b y

t h e

t m o A B C D E

g e n e s ) [ 5 1 ] . T h e s e t w o e n z y m e

c o m p l e x e s h a v e th r e e p r o t e i n s u b u n i t s in c o m -

m o n [51 ]. F u r t h e r m o r e , t h e T m o C f e r r e d o x i n a n d

T o d B f e r r e d o x i n o f t h e a r o m a t i c r i ng d io x y g e -

n a s e s s h a r e 3 2 a m i n o a c i d s e q u e n c e i d e n t i ty

a n d t h e r e f o r e m a y b e o f s im i l a r e v o l u t i o n a r y o r i -

g i n [ 51 ]. A n o t h e r c l a s s o f m o n o o x y g e n a s e a c ti v i-

t i e s is f o u n d i n e n z y m e s w h i c h o x i d i z e a lk y l s i d e

g r o u p s o n a r o m a t i c r i ng s , su c h a s x y l e n e m o n o -

o x y g e n a s e [5 2] a n d t o l u e n e s u l f o n a t e m e t h y l m o -

n o o x y g e n a s e [5 3]. T h e s e t w o e n z y m e s h a v e b i o -

c h e m i c a l l y d i s ti n c t p r o p e r t i e s , h o w e v e r , a n d d o

n o t a p p e a r s t r o n g l y r e l a t e d [ 5 3 ] .

S e v e r a l o t h e r e n z y m a t i c s t e p s a r e r e q u i r e d t o

c o n v e r t a r o m a t i c s u b s t r a t e s t o t h e h y d r o x y l a t e d

i n t e r m e d i a t e s . V e r y i n t e r e s t i n g f r o m a n e v o l u -

t i o n a r y p o i n t o f vi e w a r e t h e e x t r a d i o l c l e a v a g e

e n z y m e s , 2 , 3 - d i h y d r o x y b i p h e n y l 1 , 2 - d i o x y g e n a s e

( B p h C ) [ 54 ] a n d 1 , 2 - d i h y d r o x y n a p h t h a l e n e d i o x y -

g e n a s e ( N a h C ) [ 3 3 ] , w h i c h s h a r e s i g n i f i c a n t o v e r -

a l l a m i n o a c i d s e q u e n c e s i m i l a r i ty w i t h t h e c a t e -

c h o l 2 ,3 - d i o x y g e n a s e s X y l E , N a h H [ 33 ] a n d D m p B

[ 5 5 ] . O t h e r e x t r a d i o l c l e a v a g e e n z y m e s s u c h a s

2 , 2 ' , 3 - t r i h y d r o x y b i p h e n y l d i o x y g e n a s e [ 5 6 ] m a y

a l s o b e l o n g t o t h i s l a r g e p r o t e i n f a m i l y . D e h y d r o -

g e n a s e s c a t a l y z e t h e r e d u c t i o n o f t h e d i h y d r o d i o l

c o m p o u n d s f o r m e d b y t h e a c t i vi ty o f th e a r o m a t i c

r i n g d i o x y g e n a s e s t o f o r m c a t e c h o l s . T h e s e d e h y -

d r o g e n a s e s w e r e s h o w n t o b e r e l a t e d t o o n e a n -

o t h e r a n d t o b e l o n g t o t h e f a m i l y o f s h o r t - c h a i n

a l c o h o l d e h y d r o g e n a s e s [ 5 7 ] . U n i q u e e n z y m e a c -

t i v i t i e s f o u n d i n t h e f i r s t s t e p s o f a r o m a t i c

m e t a b o l i s m m a y h a v e b e e n r e c r u i t e d i n t o t h e s e

p a t h w a y s f r o m y e t u n k n o w n e v o l u t i o n a r y o ri g i n ,

e . g . d e h a l o g e n a t i n g e n z y m e s ( 4 - c h l o r o b e n z o a t e

d e h a l o g e n a s e o f

P s e u d o m o n a s

s p . C BS 3 [58 ] o r

d e h y d r o c h l o r i n a s e o f P. paucimobi l i s UT6 [59 ] .

I n c o n c l u s i o n , s e v e r a l c l a s s e s o f e n z y m e s c a t -

a l y z i n g t h e e a r l y s t a g e s o f t r a n s f o r m a t i o n o f a r o -

m a t i c c o m p o u n d s a r e f o u n d ( F i g. 1). E n z y m e s

w i t h i n t h e s e c l a s s e s , s u c h a s t h e m u l t i - c o m p o n e n t

d i o x y g e n a s e s , s h a r e s i g n i f i c a n t s e q u e n c e s i m i l a r i -

t ie s w i t h o n e a n o t h e r . S o m e o f t h e m , e .g . th e

e x t r a d i o l d i o x y g e n a s e s a p p e a r t o f o r m e v o l u t i o n -

a r y r e l a t e d p r o t e i n f a m i l i e s w i t h e n z y m e s f r o m

' d e e p e r ' m e t a b o l i c b r a n c h e s , s u c h a s c a t e c h o l

2 , 3 - d i o x y g e n a s e . T h i s e v o l u t i o n a r y r e l a t e d n e s s

a n d t h e g e n e t i c o r g a n i z a t i o n o f c a t a b o l i c g e n e

c l u s t e r s [ 6] s u g g e s t g e n e t i c p r o c e s s e s b y w h i c h

D N A f r a g m e n t s c o n t a i n i n g s e v e r a l g e n e s ( s o m e -

t i m e s r e f e r r e d t o a s ' g e n e m o d u l e s ' o r ' g e n e

c a s s e t t e s ' ) o r g e n e f r a g m e n t s a r e c o m b i n e d t o

f o r m n e w m e t a b o l i c p a t h w a y s o r p r o t e i n a c t i v i -

t ie s . A n e x a m p l e o f t h e e x i s t e n c e o f s u c h g e n e

m o d u l e s m a y b e a D N A f r a g m e n t c o n t a i n in g t h e

g e n e s f o r t h e a r o m a t i c r i n g d i o x y g e n a s e a n d t h e

b e n z e n e g l y c o l d e h y d r o g e n a s e ( F i g . 2 ). T h e s e

g e n e s c a n b e f o u n d a t t o t a l l y d i f f e r e n t p o s i t i o n s

i n t h e g e n o m e s o f d i f f e r e n t b a c t e r i a [6 ]. O t h e r

e x a m p l e s o f s o m e p u t a t i v e g e n e m o d u l e s w i t h in

a r o m a t i c d e g r a d a t i o n p a t h w a y s , a r e t h e m e t a


6/11

2 4 4

c l e a v a g e p a t h w a y g e n e s ( i n s tr i c t e r se n s e ) a n d t h e

g e n e s f o r a m o d i f i e d ortho c l e a v a g e p a t h w a y .

T h e meta c l e a v a g e p a t h w a y g e n e s h a v e b e e n

f o u n d i n a l m o s t i d e n t i c a l g e n e t i c o r g a n i z a t i o n a s

p a r t o f t h e o p e r o n s f o r sa l ic y l a te d e g r a d a t i o n

nah g e n e s) , t o l u a te a n d m e t a t o l u a t e d e g r a d a t i o n

( x y l g e n e s ) , p h e n o l d e g r a d a t i o n dmp g e n e s ) , a n d

t o l u e n e d e g r a d a t i o n tod g e n e s ) [ 6 ] . T h e r e a c -

t i o n s c a t a l y z e d b y t h e s e g e n e m o d u l e s a r e s h o w n

in Fig. 2.

E v o l u t i o n o f t h e c h l o r o c a t e c h o l o x i d a t i v e p a t h w a y

A n i m p o r t a n t c e n t r a l p a t h w a y f o r t h e a r o m a t i c

d e g r a d a t i o n o f c h l o r i n a t e d c o m p o u n d s in b a c te -

r i a i s t h e c h l o r o c a t e c h o l o x i d a t i v e p a t h w a y o r

m o d i f i e d o r t h o c l e a v a g e p a t h w a y [ 2 , 4 1 , 6 0 ] . C h l o -

r i n a t e d c a t e c h o l s a r e c o n v e r t e d b y a s p e c i fi c s e t

o f e n z y m e s t o f i n a l l y 3 - o x o a d i p a t e [ 6 1 , 6 2 ] , w h i c h

m a y c a r r y o n e c h l o r i n e a t o m , d e p e n d i n g o n t h e

a m o u n t o f c h l o r i n e s u b s t i t u c n t s o n t h e c a t e c h o l .

C h l o r o c a t e c h o l 1 , 2 -d i o x y g e n a se , t h e f i rs t e n z y m e

o f t h e p a t h w a y , is a n e n z y m e t h a t is a p p r o x i-

m a t e l y 4 0 i d e n t i c a l t o t h e n o r m a l c a t e c h o l 1 ,2 -

1 Arom otic r in g dioxygenose /dehydrogenose

NADII+H* NAD ~

O H

f~ ~H

NAD*

OH

NADH W

2 M o d i f i e d o r t h o c l e a v o g e p o th w o y

e l C l ) H C O O H

3 . M e t o c l e a v o g e p o t h w o y

o

~OH ~

H a C O O H

> ~oo >

O H H

R HO O ~- .C~cH J R

H

F i g. 2 . M e t a b o l i c r e a c t i o n s c a t a l y z e d b y e n z y m e s e n c o d e d o n

t h r e e p u t a t i v e g e n e m o d u l e s . O p e n a r r o w s b e t w e e n d i f f e r e n t

i n t e r m e d i a t e s i n d i c a t e t h a t m o r e t h a n o n e e n z y m a t i c s t e p is

r e q u i r e d , c l o s e d a r r o w s d e p i c t s i n g l e e n z y m a t i c s t e p s . B l a c k

a r r o w s i n d i c a t e t h e c l e a v a g e s it e f o r t h e c a t e c h o l d i o x y g e n a s e .

d i o x y g e n a s e , b u t t h a t h a s a m u c h w i d e r s u b s t r a t e

r a n g e w i t h r e s p e c t t o c o n v e r s i o n o f c h l o r o c a t e -

c h o l s [3 0 ,6 3 ]. C h l o r o m u c o n a t e c y c l o i s o m e r a s e , t h e

n e x t e n z y m e i n t h e p a t h w a y , c a n h a v e v e r y d i f f e r -

e n t s u b s t r a t e s p e c i f i c it i es d e p e n d i n g o n t h e s t r a in

f r o m w h i c h i t w a s i s o l a t e d [ 64 ]. C h l o r o m u c o n a t e

c y c l o i s o m e r a s e s h a v e a h i g h s e q u e n c e s i m i l a r i t y

t o t h e m u c o n a t e c y c l o i s o m e r a s e ( a p p r o x i m a t e -

ly 4 0 o v e r a l l a m i n o ac i d s e q u e n c e i d e n ti t y )

[3 0]. S o m e c h l o r o m u c o n a t e c y c l o i s o m e r a s e s a r e

t h o u g h t t o h a v e a n a c t i v e d e c h l o r i n a t i o n m e c h a -

n i s m , a s o p p o s e d t o t h e s p o n t a n e o u s d e c h l o r i n a -

t i o n in th e c o n v e r s i o n o f 3 - c h l o r o m u c o n a t e b y

m u c o n a t e c y c l o i s o m e r a s e . T h e c h l o r o d i e n e l a c -

t o n e s w h i c h a r e f o r m e d b y t h e a c t iv i ty o f c h l o r o -

m u c o n a t e c y c l o is o m e r a s e a r e t h e n f u r t h e r t ra n s -

f o r m e d b y d ie n e l a c t o n e h y d r o l a s e a n d b y m a l e y-

l a c e t a te r e d u c t a s e . T h e l a tt e r e n z y m e m a y a l so

h a v e a d e c h l o r i n a t i n g a c t i v it y [ 62 ].

T h e g e n e t i c o r g a n i z a t io n o f th e c h l o r o c a t e c h o l

o x i d a t i v e p a t h w a y d i f f e r s s u b s t a n t i a l l y f r o m b o t h

t h a t o f t h e n o r m a l ortho c l e a v a g e p a t h w a y , s u c h

a s t h a t c h a r a c t e r i z e d f r o m Acinetobacter cal-

coaceticus, a n d t h a t o f th e p r o t o c a t e c h u a t e p a t h -

w a y [ 1 4 , 3 5 , 3 6 , 4 4 ] . I n t h e n o r m a l ortho c l e a v a g e

p a t h w a y , catA e n c o d i n g c a t e c h o l 1 , 2 - d io x y g e n a s e ,

is s e p a r a t e d f r o m t h e o t h e r g e n e s o f t h e p a t h w a y

( F ig . 3A ) . T h e o n l y g e n e s i n t h e p r o t o c a t e c h u a t e

p a t h w a y w i t h s i g n i f i c a n t s i m i l a r i ty t o t h o s e o f t h e

m o d i f i e d ortho p a t h w a y g e n e s , a r e t h e pcaHG

g e n e s e n c o d i n g t h e p r o t o c a t e c h u a t e 3 , 4 - d i o x y -

g e n a s e ( F i g . 3 B ) . H o w e v e r , t h e s e s h o w e v e n l e s s

c o n s e r v a t i o n i n t h e i r l o c a l i z a ti o n w i t h in t h e p a t h -

w a y g e n e c l u s t e rs ( F ig . 3 B ) . I n t h e c h l o r o c a t e c h o l

o x i d a t i v e p a t h w a y , t h e g e n e e n c o d i n g t h e c h l o r o -

c a t e c h o l 1 , 2 - d i o x y g e n a s e is d i r e c t l y c o u p l e d t o

t h e c h l o r o m u c o n a t e c y c l o i s o m e r a s e g e n e [ 30 ]. In -

t e r e s ti n g l y , o n l y t h e s e t w o g e n e s a r e c o m m o n t o

t h e ortho a n d m o d i f i e d ortho p a t h w a y s . A f t e r

t h e s t a g e o f t h e c y c l o i s o m e r a s e , t h e p a t h w a y s

d i v e r g e . I n t h e o p e r o n s f o r t h e c h l o r o c a t e c h o l

o x i d a t i v e p a t h w a y , w e f i n d e v i d e n c e f o r D N A

r e a r r a n g e m e n t s a f t e r t h e c h l o r o m u c o n a t e c y c l o -

i s o m e r a s e g e n e [ 30 ]. T w o o f t h e t h r e e d i f f e r e n t

c h a r a c t e r i z e d o p e r o n s h a v e a n e x t r a D N A f r a g -

m e n t b e t w e e n t h e g e n e s e n c o d i n g c h l o r o m u -

c o n a t e c y c l o i s o m e r a s e a n d d i e n e l a c t o n e h y d r o -

l as e , w h e r e a s t h e o t h e r h a s o n l y r e m n a n t s o f th i s


7/11

245

D N A f r a g m e n t . I t c o u l d b e t h a t t h e f ir s t p a r t o f

t h e o p e r o n , i .e . t h e c h l o r o c a t e c h o l 1 , 2 - di -

o x y g e n a s e a n d c h l o r o m u c o n a t e c y c l o i s o m e r a s e

g e n e s , b e c a m e f u s e d w i t h a d if f e r e n t s e t o f g e n e s

f r o m a n o t h e r o r i g in , s i n c e t h e l a t t e r g e n e s h a v e

n o a p p a r e n t s e q u e n c e h o m o l o g y w i th g e n e s fr o m

t h e n o r m a l ortho c l e a v a g e p a t h w a y .

A s p e c i a l c a s e i s r e q u i r e d f o r th e d i f f e r e n t

r e g u l a t o r y g e n e s w h i c h a r e i n v o l v e d i n t h e r e g u l a -

t i o n o f t h e ( c h l o r o ) c a t e c h o l o x i d a t i v e p a t h w a y s .

R e g u l a t o r y g e n e s f o r t h e ortho c l e a v a g e p a t h w a y s

i n c l u d e catM (A. calcoaceticus) [65] , catR (P.

put ida)

[66 ,67 ] ,

tcbR (Pseudomonas

s p . s t r a i n P 5 1 )

[31] , clcR (P. putida p A C 2 7 ) [ 6 8 ] , a n d t fdS (Al -

caligenes eutrophus J M P 1 3 4 ) [ 69 ,7 0] . A l l e n c o d e

p r o t e i n s w h i c h b e l o n g t o t h e g r o u p o f L y s R t r a n -

s c r i p t i o n a l a c t i v a t o r s a n d a r e l o c a t e d a t a s i m i l a r

p o s i t i o n w i th r e s p e c t t o t h e r e s t o f t h e p a t h w a y

g e n e s w h i c h t h e y r e g u l a t e ( F i g . 3 ), s u g g e s t i n g th a t

t h e y f or m a n a n c i e n t t y p e o f r e g u la t i o n . A l t h o u g h

C a t R a n d C I c R r e s p o n d t o t h e in d u c e r m u c o n a t e ,

i t is n o t k n o w n t o w h a t e x t e n t t h e v a r i o u s r e g u l a -

t o r s d i f f e r in t h e i r i n d u c e r s p e c i f i c i t y o r i n r e c o g -

n i t io n o f D N A - b i n d i n g s i t es a t t h e o p e r a t o r . I t

w i ll b e i n t e r e s t i n g t o f u r t h e r a n a l y z e c h a n g e s t h a t

m a y h a v e o c c u r r e d in th e d i f f e r e n t m o d i f i e d

ortho c l e a v a g e p a t h w a y s b e f o r e t h e y o b t a i n e d

t h e i r fi n a l f o r m a n d t o d e t e r m i n e t h e p o s s i b l e

o r i g i n a l s u b s t r a t e s f o r t h is p a t h w a y i n b a c t e r i a .

o n c l u d i n g r e m a r k s

C o m p a r a t i v e s t u d ie s i n b a c t e r i a h a v e r e v e a l e d

e v i d e n c e o f e v o l u t io n a r y p r o c e s s e s t h a t c r e a t e d

o r m o d i f i e d d i f f e r e n t m e t a b o l i c p a t h w a y s , e . g.

f

B

o O O O ?

COOH

catA M B C

t i N L i

O H H O O C I ~ c o

C I~ O H ~ CI

O H

E F D

b

I I I

pea E F D B C H G~

i i

i ~ e

COOH

B D C E H G

4 I I ~ 4 - - - = q - - I - 4 - - ~

HOOC CI

CI OH

tcbR C D off E F

HOOC CI

OH

CI COOH

c l c R B

orf

HOOC e l

e , ~ o H

C Lo

Fig. 3. Comparison of the genetic organization of the different ortho cleavage pathways and reaction s catalyzed by the intradio l

dioxygenases. (A) Norm al ortho cleavage pathway encoded by the catA, catM, and catBCEFD genes of A. calcoaceticus [14,15,65].

(B) Protocatechuate pathway genes of A. calcoaceticus and of P. putida (below) [35,36,94]. (C) Modified ortho cleavage pathways

encoded by the tcbCDEF operon of Pseudomonas sp. strain P51 [29-31l, clcABD of P. putida (pAC27) [40,68], and tfdCDEF of A.

eutrophus JM PI34 [38,39]. The genes enco ding the intrad iol cleavage enzymes a re shown in black; the rea ctions these enzymes

catalyze ar e d epicte d inside the panels. A sm all arrow indicates a side rea ction with less efficiency. Arrow s directly above the gene

clusters indicate the direction of transcription. Similar shadings in the genes rep resen t significant sequence similari ties between the

genes.


8/11

246

t h o s e f o r d e g r a d a t i o n o f x e n o b i o t i c c o m p o u n d s .

I t h a s b e c o m e c l e a r t h a t s o m e s p e c i a l i z e d f u n c -

t i o n s , e .g . e n z y m e s f o r c o n v e r s i o n o f c h l o r i n a t e d

a r o m a t i c s , p r o b a b l y e v o l v e d p r i o r to t h e i n t r o d u c -

t i o n o f x e n o b i o t i c s i n t o th e e n v i r o n m e n t . O n t h e

o t h e r h a n d , n e w e v o l u t i o n a r y e v e n t s s u c h a s h o r i -

z o n t a l g e n e t r a n s f e r p r o c e s s e s o r p o i n t - m u t a t i o n s

a r e s t il l t a k i n g p l a c e a n d c a n h a v e a n i m p o r t a n t

i m p a c t o n t h e a d a p t i b i l i t y o f s t r a i n s . T h e q u e s t i o n

o f w h e t h e r t h e o c c u r r e n c e o f l a r g e q u a n t i t i e s o f

s y n t h e t i c , t o x i c c o m p o u n d s h a s l e d t o a r a p i d

e v o l u t i o n o f n e w b a c t e r i a l g e n o t y p e s , h o w e v e r , i s

s t i ll o p e n . S e v e r a l s t u d i e s h a v e r e c e n t l y i n d i c a t e d

t h a t m u t a t i o n s w o u l d b e p o s s i b l e i n b a c t e r i a w h i c h

a r e e n v i r o n m e n t a l l y i n d u c e d [ 7 1 - 7 6 ] , a l t h o u g h

t h e i s s u e i s s u b j e c t t o d e b a t e [ 7 7 ,7 8 ] . I t w i l l b e

v e r y in t e r e s t i n g t o f i n d m o r e e v i d e n c e o f r e g u l a -

t o r y c i rc u i t s in b a c t e r i a t h a t , s e n s i n g c h a n g i n g

e n v i r o n m e n t s [ 79 ] o r t h e p r e s e n c e o f t o x ic c o m -

p o u n d s [ 8 0, 81 ] , s w i t c h o n m e c h a n i s m s l e a d i n g t o

f a v o r a b l e g e n e t i c a l t e r a t i o n s .

cknowledgement

1 w o u l d l ik e t o t h a n k F l y n n P i c a r d a l f o r c r i t i c a l

r e v i e w o f t h e m a n u s c r i p t .

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