Pesticides in the Soil Microbial Ecosystem - ACS Publications

Chapter 1

Pesticides in the Soil Microbial Ecosystem Kenneth D. Racke

Downloaded by 79.110.25.167 on January 21, 2017 | http://pubs.acs.org Publication Date: May 3, 1990 | doi: 10.1021/bk-1990-0426.ch001

Environmental Chemistry Laboratory, DowElanco, 9001 Building, Midland, MI 48641-1706

The soil environment comprises a diverse ecosystem in which the recycling of organic matter provides a key link with global carbon and nutrient cycles. Soil contains populations of microorganisms that have exceptional degradative capabilities and the ability to adapt to utilize the variety of allochthonous organic materials that enter the soil carbon cycle. As man has come to rely upon the use of soil-applied pesticides in many agroecosystems, he has learned that the residual control provided by these compounds is modulated by both abiotic and biotic degradative processes. The ability of microorganisms to adapt for rapid catabolism of some soil pesticides has in some cases resulted in economically significant pest control failures. The phenomenon of enhanced pesticide degradation has become a significant concern requiring the development of management strategies. Yet, this unwelcome occurrence has led to valuable opportunities to investigate the remarkable adaptability and complexity of the soil microbial ecosystem.

In o r d e r t o p r o p e r l y u n d e r s t a n d p e s t i c i d e s i n t h e c o n t e x t o f t h e s o i l m i c r o b i a l ecosystem, i t i s important t o c o n s i d e r t h e r e l e v a n t p r o p e r t i e s o f t h e s o i l environment, t h e m e t a b o l i c c a p a b i l i t i e s o f t h e s o i l m i c r o b i a l community, and t h e uses and d i s s i p a t i o n r o u t e s o f soil-applied pesticides. The

Soil

Environment

S o i l has been d e f i n e d as t h e " u n c o n s o l i d a t e d m i n e r a l m a t e r i a l on t h e immediate s u r f a c e o f t h e e a r t h t h a t s e r v e s a s a n a t u r a l medium f o r the growth o f l a n d p l a n t s " (1). A l t h o u g h t h i s sounds r e l a t i v e l y 0097-6156/90/0426-0001S06.00/0 © 1990 American Chemical Society

Racke and Coats; Enhanced Biodegradation of Pesticides in the Environment ACS Symposium Series; American Chemical Society: Washington, DC, 1990.


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s i m p l e , i n r e a l i t y s o i l i s a complex ecosystem, not m e r e l y the " d i r t " of v e r n a c u l a r language. In a p h y s i c a l sense, s o i l i s composed o f m i n e r a l m a t e r i a l ( c l a y , s i l t , sand, s t o n e s ) , a i r o r w a t e r - f i l l e d p o r e space, and o r g a n i c matter. The s o i l o r g a n i c m a t t e r i s a v e r y important and a c t i v e component. Roughly t h r e e f r a c t i o n s c a n be d e l i n e a t e d ; a m a c r o s c o p i c component composed o f p a r t i c u l a t e p l a n t and animal d e b r i s i n e a r l y s t a g e s o f breakdown , a c h e m i c a l l y w e l l d e f i n e d assemblage o f v a r i o u s s i m p l e o r g a n i c compounds ( c a r b o h y d r a t e s , amino a c i d s , p r o t e i n s ) , and a complex, d a r k - c o l o r e d component, l a r g e l y a r o m a t i c and p o l y m e r i c ( i . e . , "humus"), t h a t i s r e l a t i v e l y r e s i s t a n t to degradation (2). Turnover times f o r o r g a n i c d e b r i s , s o l u b l e compounds, and humus a r e on the o r d e r o f 2-5 y e a r s , 5-25 y e a r s , and 250-2500 y e a r s , r e s p e c t i v e l y ( 3 ) . The p h y s i c a l components o f s o i l a r e i n t e g r a t e d i n t o a h e t e r o g e n e o u s m a t r i x t h a t forms the b a s i s f o r the s o i l a g g r e g a t e and p a r t i c l e . F o r example, c l a y s and humic m a t e r i a l s a r e o f t e n i n t i m a t e l y a s s o c i a t e d t o f o r m o r g a n o - m i n e r a l complexes ( 4 ) . The s o i l s h o u l d be u n d e r s t o o d as an ecosystem, w i t h p o p u l a t i o n s o f m i c r o s c o p i c ( b a c t e r i a , f u n g i , p r o t o z o a n s , a l g a e ) and m a c r o s c o p i c ( a n n e l i d s , a r t h r o p o d s ) organisms f o r m i n g complex f o o d web communities. The s o i l m i c r o f l o r a p l a y a key r o l e i n g l o b a l l y significant nutrient cycles. Important examples o f s u c h microbially-mediated processes are n i t r i f i c a t i o n , d e n i t r i f i c a t i o n , and c a r b o n m i n e r a l i z a t i o n . The s o i l e c o s y s t e m c o n s t i t u t e s an a l l o c h t h o n o u s one i n an e n e r g e t i c sense, w i t h p l a n t and animal d e b r i s e n t e r i n g the s o i l t o b e g i n the d e g r a d a t i v e p r o c e s s . In a p r a c t i c a l sense, the s o i l may be viewed as a v a s t r e c y c l i n g depot, c o n t i n u a l l y r e c e i v i n g r e d u c e d compounds o f c a r b o n and c o n t i n u a l l y o x i d i z i n g them to C02 and water ( 5 ) . Of the s o i l o r g a n i s m s a c t i v e i n t h i s r e c y c l i n g e f f o r t , the s o i l f u n g i a r e p a r t i c u l a r l y e f f e c t i v e i n i n i t i a t i n g the d e g r a d a t i o n o f r a t h e r complex p o l y m e r i c s u b s t r a t e s (e.g., c e l l u l o s e ) , whereas the s o i l b a c t e r i a have i n g e n e r a l s p e c i a l i z e d i n the degradation of simpler, soluble organics. Among the i n d i g e n o u s p o p u l a t i o n s a r e many b a c t e r i a l s p e c i e s t h a t a r e l a r g e l y q u i e s c e n t , but f l o u r i s h d r a m a t i c a l l y when r e a d i l y a v a i l a b l e o r g a n i c n u t r i e n t s a r e added ( 6 ) . Thus, a l t h o u g h the s o i l has o f t e n been viewed as a r i c h , f e r t i l e ecosystem, i n r e a l i t y s o i l i s c o n s i d e r e d t o be an o l i g o t r o p h i c environment ( 7 ) . The f i e r c e n a t u r e o f c o m p e t i t i o n f o r the e a s i l y d e g r a d a b l e o r g a n i c compounds added t o s o i l i s e x e m p l i f i e d by a n t i b i o t i c p r o d u c t i o n by s o i l m i c r o o r g a n i s m s , which p r o b a b l y r e p r e s e n t s a f o r m o f c h e m i c a l w a r f a r e o v e r the d e f e n s e o f n i c h e s ( 6 ) . P e s t i c i d e s A p p l i e d t o the S o i l

Environment

S o i l i s the f o u n d a t i o n o f a g r i c u l t u r e . I t i s the s u b s t r a t e i n which the agronomic c r o p s o f the e a r t h f i n d r e q u i r e d n u t r i e n t s , water, m i c r o b i a l symbionts, and a p h y s i c a l anchor. Due t o t h e p r e s e n c e i n s o i l o f c r o p c o m p e t i t o r s and c o m p e t i t o r s f o r the use o f t h i s p l a n t biomass, p e s t i c i d e s have become i n d i s p e n s i b l e t o o l s i n t h e management o f weeds, i n s e c t s , and f u n g i o f economic s i g n i f i c a n c e . At p r e s e n t t h e r e a r e a p p r o x i m a t e l y 600 d i f f e r e n t p e s t i c i d e a c t i v e i n g r e d i e n t s r e g i s t e r e d f o r use i n the U.S., and m i l l i o n s o f pounds a r e g l o b a l l y a p p l i e d e a c h y e a r , w i t h the w o r l d market e s t i m a t e d a t g r e a t e r t h a n 20 b i l l i o n d o l l a r s ( 8 ) . Much o f t h i s use r e p r e s e n t s d i r e c t a p p l i c a t i o n to s o i l , and a c o n s i d e r a b l e p o r t i o n o f t h a t which i s f o l i a r l y a p p l i e d



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Pesticides in the Soil Microbial Ecosystem

may r e a c h t h e s o i l as s p r a y d r i f t , r u n o f f , o r wash-off. One c o n s i d e r a t i o n o f the use o f s o i l - a p p l i e d p e s t i c i d e s i s t h a t t h e y s h o u l d p e r s i s t l o n g enough i n s o i l t o c o n t r o l t h e t a r g e t p e s t ( s ) , but not so l o n g as t o c r e a t e e n v i r o n m e n t a l r i s k s . H e r b i c i d e s which a r e a p p l i e d d i r e c t l y t o s o i l w i t h the i n t e n t o f p r o v i d i n g r e s i d u a l weed c o n t r o l may be a p p l i e d p r i o r t o c r o p p l a n t i n g ( p r e p l a n t ) o r a f t e r p l a n t i n g and p r i o r t o weed emergence (preemergence). Classes of h e r b i c i d e s that are a p p l i e d preplant or preemergence i n c l u d e the t r i a z i n e s , s u b s t i t u t e d u r e a s , carbamates, c a r b a m o t h i o a t e s , s u l f o n y l u r e a s , c h l o r a c e t a r n i d e s , and d i n i t r o a n i l i n e s (9). Many i m p o r t a n t c r o p s , s u c h as c o r n and soybeans, r e l y upon p r e p l a n t o r preemergence h e r b i c i d e s . A t y p i c a l preemergent weed c o n t r o l s c e n a r i o i s p r o v i d e d by the o c c u r r e n c e o f w i l d p r o s o m i l l e t (Panicum miliaceum) i n Midwestern U.S. c o r n . Wild proso m i l l e t i s a p e r n i c i o u s g r a s s s p e c i e s , and o f t e n e x h i b i t s b o t h e a r l y and l a t e s e a s o n f l u s h e s (10). One o f the h e r b i c i d e s t h a t i s e f f e c t i v e a g a i n s t t h i s weed i s EPTC, which must be f o r m u l a t e d w i t h a m e t a b o l i c s a f e n e r ( d i c h l o r m i d ) t h a t a l l o w s c o r n t o escape i t s h e r b i c i d a l e f f e c t s . EPTC i s a p p l i e d p r e p l a n t - i n c o r p o r a t e d a t 2.2-6.7 kg/ha and must p e r s i s t i n s i g n i f i c a n t q u a n t i t i e s f o r r o u g h l y 15-30 days f o r e f f e c t i v e c o n t r o l o f e a r l y s e a s o n f l u s h e s o f w i l d p r o s o m i l l e t (11.). s h o u l d be n o t e d t h a t i n many agroecosysterns, s u c h as c o r n , h e r b i c i d e s o r "tank mixes" o f m u l t i p l e h e r b i c i d e s a r e a p p l i e d t o c o n t r o l complexes o f weed s p e c i e s . J t

A l t h o u g h t h e use o f i n s e c t i c i d e s i s not as h e a v i l y skewed toward s o i l a p p l i c a t i o n as t h a t f o r h e r b i c i d e s , t h e r e a r e s e v e r a l s i g n i f i c a n t c r o p s s u c h as c o r n , peanuts, and s u g a r b e e t s which r e l y h e a v i l y on s u c c e s s f u l c o n t r o l o f s o i l i n s e c t p e s t s . A typical example o f s o i l i n s e c t p e s t c o n t r o l i s p r o v i d e d by the c o r n rootworm (Diabrotica spp.). T h i s key p e s t o f c o r n o v e r w i n t e r s i n the egg s t a g e i n c o r n s t u b b l e , and a f t e r a v a r i a b l e h a t c h i n g p e r i o d the l a r v a e a c t i v e l y damage c o r n r o o t s from e a r l y June t o l a t e J u l y (12). The most common method o f c o r n rootworm c o n t r o l i n v o l v e s an a t - p l a n t i n g (April-May) a p p l i c a t i o n of a granular i n s e c t i c i d e , such as c a r b o f u r a n , a t 1 kg/ha. To p r o v i d e e f f e c t i v e rootworm c o n t r o l the c a r b o f u r a n a p p l i e d must p e r s i s t i n t o x i c c o n c e n t r a t i o n s f o r a p p r o x i m a t e l y 4-8 weeks a f t e r a p p l i c a t i o n (13). Insecticides of s e v e r a l c l a s s e s have been employed f o r s o i l i n s e c t c o n t r o l , i n c l u d i n g organophosphorus, carbamate, and p y r e t h r o i d compounds. F u n g i c i d e s a r e a p p l i e d t o s o i l i n a few s p e c i f i c i n s t a n c e s f o r c o n t r o l o f s o i l - b o r n e p l a n t pathogens. Some c r o p s f o r which s o i l - a p p l i e d f u n g i c i d e a p p l i c a t i o n s are o f t e n necessary include o n i o n s , peanuts, and avocado. An example o f t h i s would be the use o f i p r o d i o n e f o r the c o n t r o l o f w h i t e r o t d i s e a s e {Sclerotium cepivorum) o f o n i o n s i n the U n i t e d Kingdom (14). S o i l - a p p l i e d f u n g i c i d e s are o f t e n s y s t e m i c i n n a t u r e , and may need t o be t a k e n up by p l a n t r o o t s and t r a n s l o c a t e d t o stem and f o l i a g e f o r e f f i c a c i o u s pathogen control. S e v e r a l commonly used s o i l f u n g i c i d e s a r e i p r o d i o n e , carbendazim, and thiabendazole. Mechanisms o f P e s t i c i d e D i s s i p a t i o n i n S o i l P e s t i c i d e s which a r e a p p l i e d t o s o i l become enmeshed i n the t r a n s p o r t and d e g r a d a t i o n p r o c e s s e s t h a t a f f e c t a l l a l l o c h t h o n o u s organics added t o t h i s dynamic e c o s y s t e m (15).



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Transport Processes. There a r e s e v e r a l p r o c e s s e s t h a t a r e a c t i v e i n t r a n s p o r t i n g p e s t i c i d e r e s i d u e s w i t h i n o r o u t o f t h e s o i l ecosystem. The f i r s t c l a s s o f p r o c e s s e s i n v o l v e s a e r i a l t r a n s p o r t o f p e s t i c i d e s f r o m t h e s o i l i n t o t h e atmosphere. V o l a t i l i z a t i o n i s an important p r o c e s s by which p e s t i c i d e s i n t h e v a p o r phase c a n move f r o m t h e s o i l s u r f a c e i n t o t h e atmosphere. P e s t i c i d e s with vapor p r e s s u r e s g r e a t e r t h a n a p p r o x i m a t e l y 10" mm Hg a t 25°C a r e most g r e a t l y a f f e c t e d , and l o s s e s f r o m s u r f a c e a p p l i c a t i o n s c a n a p p r o a c h g r e a t e r t h a n 50% i n l e s s t h a n 48 h o u r s (16). In a d d i t i o n t o the vapor p r e s s u r e o f a p e s t i c i d e , which i n c r e a s e s w i t h i n c r e a s i n g temperature, s e v e r a l s o i l p r o p e r t i e s s u c h as m o i s t u r e and o r g a n i c m a t t e r c o n t e n t c a n g r e a t l y modify the k i n e t i c s o f v o l a t i l i z a t i o n . T h i s i s due t o t h e f a c t t h a t p e s t i c i d e s i n s o i l p a r t i t i o n between a t l e a s t t h r e e phases: s o i l - s o r b e d , s o i l s o l u t i o n , and s o i l a i r (17). Although not i n t e n s i v e l y i n v e s t i g a t e d , movement o f s o i l p a r t i c l e s and a t t a c h e d p e s t i c i d e s by wind may a l s o p l a y a r o l e under some e n v i r o n m e n t a l conditions. The s e c o n d c l a s s o f p e s t i c i d e t r a n s p o r t p r o c e s s e s i s t h a t o f movement o f d i s s o l v e d o r p a r t i c u l a t e - s o r b e d p e s t i c i d e s i n water. L e a c h i n g o f p e s t i c i d e s has been r e c o g n i z e d a s a c r i t i c a l p r o c e s s , i f not i n t h e s e n s e o f t h e a b s o l u t e p e r c e n t a g e o f a p p l i e d p e s t i c i d e leached i n t o the s o i l p r o f i l e , then with respect t o the contamination o f groundwater by t r a c e q u a n t i t i e s o f p e s t i c i d e . S e v e r a l pathways o f d i s s o l v e d p e s t i c i d e movement w i t h l e a c h i n g water a r e r e c o g n i z e d ( 1 8 ) . C o n v e c t i o n and d i f f u s i o n a r e o f t e n s i m u l t a n e o u s p r o c e s s e s t h a t i n v o l v e p e s t i c i d e t r a n s p o r t i n water moving g r a v i t a t i o n a l l y o r w i t h a concentration gradient. Macropore f l o w i n v o l v e s p e s t i c i d e t r a n s p o r t i n water f l o w i n g t h r o u g h t h e i r r e g u l a r network o f c h a n n e l s c r e a t e d by earthworms, r o o t s , i n s e c t s , and b u r r o w i n g a n i m a l s . The e x t e n t o f l e a c h i n g i s g o v e r n e d by p a r t i t i o n i n g p r o c e s s e s between s o r b e d and s o l u t i o n phase p e s t i c i d e , and o f t e n l a b o r a t o r y - d e t e r m i n e d s o r p t i o n c o e f f i c i e n t s (e.g. F r e u n d l i c h Kd) a r e used t o p r e d i c t f i e l d l e a c h i n g p o t e n t i a l (19). An u n d e r s t a n d i n g o f t h e r e l a t i o n s h i p between o b s e r v e d p a r t i t i o n i n g b e h a v i o r and a c t u a l f i e l d l e a c h i n g measurement i s c o m p l i c a t e d by s u c h f a c t o r s as n o n e q u i 1 i b r i u m p a r t i t i o n i n g r e s u l t i n g f r o m s l o w - d e s o r p t i o n k i n e t i c s (20). Transport o f p e s t i c i d e s i n water moving o v e r t h e s o i l s u r f a c e i s a l s o a n i m p o r t a n t p r o c e s s t h a t c a n impact s u r f a c e - w a t e r q u a l i t y . P e s t i c i d e s w i t h water s o l u b i l i t i e s g r e a t e r t h a n a p p r o x i m a t e l y 10 pg/g have been h y p o t h e s i z e d t o move l a r g e l y i n t h e s o l u t i o n phase, w h i l e l e s s s o l u b l e p e s t i c i d e s a r e thought t o move m a i n l y s o r b e d t o e r o d i n g s o i l p a r t i c l e s (21). A b i o t i c Transformation Processes. P e s t i c i d e s that r e s i d e w i t h i n o r on t h e s o i l a r e s u b j e c t t o t h e a b i o t i c and m i c r o b i o l o g i c a l transformation processes that operate i n t h i s great r e c y c l i n g ecosystem. A f t e r numerous problems w i t h t h e p r o l o n g e d p e r s i s t e n c e o f some e a r l y s o i l p e s t i c i d e s (e.g. a l d r i n , c h l o r d a n e ) , d e g r a d a b i l i t y i s viewed a s a d e s i r a b l e a t t r i b u t e o f modern s o i l - a p p l i e d p e s t i c i d e s . D e g r a d a t i o n p r o c e s s e s i n s o i l may r e s u l t i n a c c u m u l a t i o n o f well-defined metabolites, incorporation o f p e s t i c i d e carbon o r n i t r o g e n i n t o t h e s o i l o r g a n i c m a t t e r f r a c t i o n , o r complete mineralization. Many o f t h e a b i o t i c d e g r a d a t i o n p r o c e s s e s a c t i v e i n s o i l r e s u l t i n p a r t i a l degradation o f the p e s t i c i d e to products that a r e f u r t h e r d e g r a d e d m i c r o b i a l l y , accumulate i n s o i l t e m p o r a r i l y , o r


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b i n d t o s o i l o r g a n i c components. Exposure o f p e s t i c i d e r e s i d u e s t o u l t r a v i o l e t r a d i a t i o n can r e s u l t i n considerable photodegradation o f p e s t i c i d e s on t h e s o i l s u r f a c e , a l t h o u g h o n l y r e s i d u e s on t h e extreme s u r f a c e l a y e r ( t e r b u f o s s u l f o x i d e ) and r e d u c t i o n s ( p a r a t h i o n =» a m i n o - p a r a t h i o n ) c a n a l s o be i m p o r t a n t t r a n s f o r m a t i o n p r o c e s s e s f o r s p e c i f i c p e s t i c i d e s (29,30).


+

M i c r o b i o l o g i c a l Transformation Processes. The importance o f t h e s o i l m i c r o b i a l community i n m e d i a t i n g p e s t i c i d e d e g r a d a t i o n has l o n g been recognized. I n f a c t , i t was f o r one o f t h e f i r s t s y n t h e t i c o r g a n i c p e s t i c i d e s , 2,4-D, t h a t m i c r o b i o l o g i c a l d e g r a d a t i o n was f i r s t shown t o be a n important f a c t o r (31). The c o n c l u s i o n o f t h i s e a r l y work was " . . . t h e d e t o x i c a t i o n o f 2 : 4 - d i c h l o r o p h e n o x y a c e t i c a c i d i n g a r d e n loam i s due almost e n t i r e l y t o t h e a c t i v i t y o f m i c r o o r g a n i s m s " . S i n c e t h i s e a r l y d i s c o v e r y t h e r e has been c o n s i d e r a b l e a p p r e c i a t i o n f o r t h e r o l e o f t h e s o i l m i c r o b i a l community i n p e s t i c i d e transformations. I n some c a s e s t h e r o l e o f m i c r o o r g a n i s m s has been s t r e s s e d by c o m p a r i s o n o f d e g r a d a t i o n r a t e s i n n a t u r a l and s t e r i l i z e d systems (32), w h i l e i n o t h e r s r e s e a r c h e r s have c h o s e n t o use i s o l a t i o n o f p e s t i c i d e - d e g r a d i n g microorganisms from s o i l as evidence o f m i c r o b i a l involvement (33). I t has a l s o been r e c o g n i z e d t h a t environmental c o n d i t i o n s that influence microbial a c t i v i t y (temperature, moisture,...) a f f e c t the m i c r o b i a l d e g r a d a t i o n o f p e s t i c i d e s i n s o i l (34). The importance o f m i c r o b i a l i n v o l v e m e n t i s d e m o n s t r a t e d by t h e many r e v i e w s o f p e s t i c i d e / m i c r o b e i n t e r a c t i o n s t h a t have a p p e a r e d (35-41). The m i c r o b i a l m e t a b o l i s m o f p e s t i c i d e s has o f t e n been s u b d i v i d e d into 2 d i s t i n c t classes. The f i r s t o f t h e s e i s termed s i m p l y "catabolism". This process o f t e n r e s u l t s i n the m i n e r a l i z a t i o n o f some p o r t i o n o f an o r g a n i c compound v i a e n z y m a t i c pathways t o s i m p l e p r o d u c t s o f u n i v e r s a l c u r r e n c y (C02, N H 3 ) . I n some c a s e s , one p o r t i o n o f t h e m o l e c u l e may be m i n e r a l i z e d and a n o t h e r p o r t i o n may accumulate i n s o i l . This i s true f o r the s o i l microbial degradation o f c a r b o f u r a n (42,43). T h e r e f o r e , c a t a b o l i s m s h o u l d n o t be e q u a t e d w i t h m i n e r a l i z a t i o n o r complete d e s t r u c t i o n o f a p e s t i c i d e . I t s h o u l d be p o i n t e d out, however, t h a t m i n e r a l i z a t i o n o f a p e s t i c i d e i n s o i l is n e a r l y always a consequence o f m i c r o b i a l a c t i v i t y (44)key t o u n d e r s t a n d i n g c a t a b o l i s m i s t h a t i t i s p r i m a r i l y a p r o c e s s d r i v e n by t h e m i c r o b i a l quest f o r energy. T h e r e f o r e , c a t a b o l i s m has come t o be e q u a t e d w i t h u t i l i z a t i o n o f a p e s t i c i d e a s a n e n e r g y s o u r c e and t h u s a growth s u b s t r a t e (40,41). C a t a b o l i s m i s most commonly l i n k e d t o t h e c o n v e r s i o n o f p e s t i c i d e s i n t o c a r b o n s k e l e t o n T


n

e


6

ENHANCED BIODEGRADATION OF PESTICIDES IN THE ENVIRONMENT

f e e d s t o c k s f o r e x i s t i n g m e t a b o l i c pathways. However, i n a few i n s t a n c e s pure c u l t u r e s o f p e s t i c i d e - d e g r a d i n g m i c r o o r g a n i s m s i s o l a t e d from s o i l have been c a p a b l e o f e x p l o i t i n g p e s t i c i d e s as s o l e s o u r c e s o f phosphorus (45,46), n i t r o g e n (42), o r s u l f u r (47). A second r e c o g n i z e d c l a s s o f m i c r o b i a l p e s t i c i d e metabolism, "cometabolism", i s r e l a t e d t o the o b s e r v e d u n c o o r d i n a t i o n o f m i c r o b i a l enzyme a c t i v i t i e s . As D a g l e y (48) has o b s e r v e d : "Most m i c r o b i a l d e g r a d a t i v e ( c a t a b o l i c ) enzymes a r e not l i n k e d directly to p r o c e s s e s t h a t h a r n e s s r e l e a s e d e n e r g y f o r growth. Thus, enzymes t h a t add water, o r break c h e m i c a l bonds by h y d r o l y s i s o r a l d o l f i s s i o n , s i m p l y s e r v e the f u n c t i o n o f s u p p l y i n g s u b s t r a t e s f o r t h e m e t a b o l i c sequences t h a t t e r m i n a t e i n e n e r g y p r o d u c t i o n " . When a d i s j u n c t i o n o c c u r s , i n c o m p l e t e p e s t i c i d e d e g r a d a t i o n r e s u l t s , and t h e r e i s an a c c u m u l a t i o n o f i n t e r m e d i a t e m e t a b o l i c p r o d u c t s . The phenomenon o f cometabolism has been d e f i n e d as the d e g r a d a t i o n " o f s u b s t a n c e s w i t h o u t u t i l i z a t i o n o f the e n e r g y d e r i v e d f r o m t h e i r o x i d a t i o n t o s u p p o r t growth..." (49). M i c r o b i o l o g i c a l s t u d i e s to d i s t i n g u i s h c a t a b o l i s m from c o m e t a b o l i s m under n a t u r a l c o n d i t i o n s a r e not t r i v i a l , and most r e s e a r c h e r s have r e l i e d upon work w i t h i s o l a t e d pure c u l t u r e s . The c o n c l u s i o n s , a p p r o p r i a t e o r not, drawn f r o m pure c u l t u r e work i n the l a b o r a t o r y depend on whether a m i c r o o r g a n i s m c a p a b l e o f growing on the p e s t i c i d e i s i s o l a t e d ( i . e . , c a t a b o l i s m ) o r not ( i . e . , c o m e t a b o l i s m ) . A new emphasis i s now b e i n g p l a c e d by r e s e a r c h e r s on u n d e r s t a n d i n g c o m e t a b o l i s m i n i t s e c o l o g i c a l c o n t e x t . T h i s r e e v a l u a t i o n has been s p u r r e d by i n s t a n c e s i n w h i c h no s i n g l e microbe c a n c a t a b o l i z e a p e s t i c i d e , but o n l y by t h e s y n e r g i s t i c i n t e r a c t i o n s o f s e v e r a l members o f a m i c r o b i a l c o n s o r t i u m i s m i n e r a l i z a t i o n and growth r e a l i z e d (50-53). Microbial

Adaptation f o r Degradation

The p a t t e r n o f m i c r o b i a l p o p u l a t i o n growth p r e s e n t s some i n t e r e s t i n g ecological implications. Because the most common mode o f b a c t e r i a l r e p r o d u c t i o n i n v o l v e s f i s s i o n , w i t h two d a u g h t e r c e l l s formed f r o m e a c h s p l i t p a r e n t , m i c r o b i a l p o p u l a t i o n s e x h i b i t t h e phenomenon o f e x p o n e n t i a l growth. The c l a s s i c growth c u r v e f o r b a c t e r i a l p o p u l a t i o n s i n v o l v e s 4 r e c o g n i z e d phases (54). The lag phase i s a p e r i o d d u r i n g which no growth o c c u r s upon p r e s e n t a t i o n o f a new carbonaceous e n e r g y s o u r c e t o the p o p u l a t i o n . T h i s l a g i s due t o t h e time n e c e s s a r y t o g e a r up the m e t a b o l i c machinery t h r o u g h enzyme and coenzyme s y n t h e s i s , a p r o c e s s which has been termed " i n d u c t i o n " . D u r i n g the exponential phase the p o p u l a t i o n grows e x p o n e n t i a l l y as i t e x p l o i t s t h e growth s u b s t r a t e . The stationary phase i s r e a c h e d when p o p u l a t i o n growth slows and h a l t s due t o l i m i t a t i o n s o f n u t r i e n t d e p l e t i o n o r t o x i n a c c u m u l a t i o n . F i n a l l y , the death phase i s c h a r a c t e r i z e d by a d e c l i n e i n the v i a b l e p o p u l a t i o n . Microbiologists have used t h i s s c e n a r i o as a paradigm o f m i c r o b i a l p o p u l a t i o n growth, y e t i t s h o u l d be n o t e d t h a t t h i s i s almost e n t i r e l y based on pure c u l t u r e work i n the l a b o r a t o r y . A l t h o u g h i n some c a s e s t h i s t y p e o f growth p a t t e r n may be o b s e r v e d i n s o i l (55), t h e r e i s some doubt whether i n the m a t r i x o f complex m i c r o b i a l community i n t e r a c t i o n s i n the h a r s h s o i l environment t h i s p a t t e r n i s as c l e a r l y d i s p l a y e d . S o i l b a c t e r i a l growth r a t e s i n n a t u r e seem t o be f a r s l o w e r t h a n t h o s e t y p i c a l o f s o i l b a c t e r i a grown i n r i c h n u t r i e n t media i n t h e l a b o r a t o r y (7). I t has been c o n c l u d e d t h a t m i c r o b i a l p o p u l a t i o n s i n



1. RACKE


7

s o i l a r e l a r g e l y dormant, w i t h o n l y 15-30% o f t h e b a c t e r i a l p o p u l a t i o n a c t i v e even under t h e most f a v o r a b l e c o n d i t i o n s (56,57). The m a j o r i t y o f e v i d e n c e p o r t r a y s s o i l b a c t e r i a l p o p u l a t i o n s a s o p e r a t i n g on what i s e c o l o g i c a l l y known a s R p o p u l a t i o n growth s t r a t e g y : p o p u l a t i o n s r a p i d l y i n c r e a s e t o e x p l o i t f a v o r a b l e growth c o n d i t i o n s ( i . e . , "boom"), and m a i n t a i n n e g l i g i b l e p o p u l a t i o n growth and a c t i v i t y d u r i n g p e r i o d s o f u n f a v o r a b l e c o n d i t i o n s ( i . e . , " b u s t " ) (Z, 58). The s o i l e c o s y s t e m i s p r i m a r i l y a n a l l o c h t h o n o u s one i n terms o f e n e r g e t i c input, r e c e i v i n g i t s energy input p r i m a r i l y as o r g a n i c c a r b o n c o n s t i t u e n t s o f p l a n t and a n i m a l d e b r i s . Plants alone i n t r o d u c e a n i n c r e d i b l e d i v e r s i t y o f compounds i n t o t h e s o i l : cellulose, hemicelluloses, lignin, starch, pectins, proteins, l i p i d s , pigments, and d e f e n s e c h e m i c a l s (e.g., n i c o t i n e , r o t e n o n e ) ( 5 9 ) . As a consequence, a n a l y s e s o f s o i l r e v e a l t h e p r e s e n c e o f a m y r i a d o f b i o c h e m i c a l l y i d e n t i f i a b l e components i n a d d i t i o n t o t h e more amorphous humic m a t e r i a l s ( 3 ) . As might be e x p e c t e d , t h e s o i l m i c r o b i a l community c o n t a i n s p o p u l a t i o n s o f f u n g i , a c t i n o m y c e t e s , and b a c t e r i a t h a t degrade t h i s d i v e r s e n u t r i t i o n a l o f f e r i n g . The f u n g a l and a c t i n o m y c e t e p o p u l a t i o n s o f t e n a c t a s p r i m a r y d e g r a d e r s i n s o i l , and a r e v e r y a c t i v e i n t h e d e g r a d a t i o n o f r a t h e r complex s u b s t r a t e s s u c h a s c e l l u l o s e , l i g n i n , and c h i t i n ( 6 ) . The s o i l b a c t e r i a l p o p u l a t i o n c o n t a i n s some organisms which have become s p e c i a l i z e d t o u t i l i z e some f a i r l y s i m p l e a l i p h a t i c and a r o m a t i c s u b s t r a t e s a s growth s u b s t r a t e s , some o f which appear t o p r e s e n t p e c u l i a r m e t a b o l i c conundrums. F o r example, a s u r v e y o f t h e Arthrobacter spp. o f agronomic s o i l s f o u n d a s p e c t r u m o f n u t r i t i o n a l s u b g r o u p i n g s represented, that i n a d d i t i o n t o t y p i c a l s u b s t r a t e s such as glucose, b u t y r i c a c i d , and g l y c i n e , c o u l d u t i l i z e s u c h compounds a s b e n z o i c a c i d , s a l i c y l i c a c i d , h i s t a m i n e , and methylamine a s s o l e c a r b o n s o u r c e s (60). The c a p a b i l i t i e s o f s e v e r a l g e n e r a o f s o i l b a c t e r i a f o r d e g r a d a t i o n o f complex, s o l u b l e s u b s t r a t e s a r e w e l l known. F o r example, Pseudomonas spp. a r e common s o i l b a c t e r i a t h a t c a n u t i l i z e many a r o m a t i c compounds f o r growth. Some o f t h e compounds d e g r a d e d i n c l u d e camphor, n a p h t h a l e n e , t o l u e n e , p h t h a l i c a c i d , and o c t a n e (61,62). The b a c t e r i a l community i s c a p a b l e o f d e g r a d i n g v i r t u a l l y any o r g a n i c compound t h a t i s added t o t h e s o i l environment, due t o some m i c r o o r g a n i s m o r m i c r o b i a l c o n s o r t i u m t h a t c a n degrade and m i n e r a l i z e t h e compound and e x t r a c t e n e r g y from i t f o r growth ( 5 ) . How c a n some p o r t i o n s o f t h e s o i l m i c r o b i a l community be s o f l e x i b l e i n t h e i r n u t r i t i o n a l r e q u i r e m e n t s so a s t o e x p l o i t t h e v a r i e t y o f c a r b o n s o u r c e s t h a t e n t e r t h e s o i l e n v i r o n m e n t ? The answer t o t h i s q u e s t i o n l i e s i n t h e u n i q u e m i c r o e v o l u t i o n a r y n a t u r e of microbial substrate adaptation. Characteristic of microbial m e t a b o l i s m i s t h e a d a p t a b i l i t y o f m i c r o o r g a n i s m s t h r o u g h m u t a t i o n and i n d u c t i o n t o d e v e l o p t h e a b i l i t y t o degrade compounds which i n i t i a l l y c o u l d n o t be degraded o r were t o x i c (63). This can involve the e v o l u t i o n o f s u i t a b l e c e l l w a l l t r a n s p o r t systems, o f more e f f i c i e n t enzymes, o r o f enzymes w i t h new a c t i v i t i e s (64). Any o f t h e s e s c e n a r i o s would c o n f e r a s e l e c t i v e advantage on t h e m i c r o o r g a n i s m i n v o l v e d , and would have s i g n i f i c a n t e c o l o g i c a l i m p l i c a t i o n s because e a c h b a c t e r i a l c e l l has t h e a b i l i t y t o f o r m an e n t i r e p o p u l a t i o n (65). One o f t h e k e y f a c t o r s i n t h e m e t a b o l i c a d a p t a b i l i t y o f m i c r o o r g a n i s m s i s r e l a t e d t o t h e p o s s e s s i o n and u t i l i z a t i o n o f plasmids. P l a s m i d s a r e extrachromosomal c i r c l e t s o f g e n e t i c m a t e r i a l



8


(DNA) t h a t i n b a c t e r i a e x i s t i n d e p e n d e n t l y o f the chromosome, and o f t e n encode f o r " n o n e s s e n t i a l " but u s e f u l c h a r a c t e r i s t i c s s u c h as c o n j u g a t i o n f a c t o r s , c a p s u l e f o r m a t i o n , h o s t s p e c i f i c i t y , and d r u g r e s i s t a n c e (66). M e t a b o l i c genes r e s i d i n g on p l a s m i d s i n c l u d e t h e a b i l i t y t o degrade camphor, t o l u e n e , naphthalene, o c t a n e , and PCB's (61,67). D e g r a d a t i v e p l a s m i d s c a n be t r a n s f e r r e d between i n d i v i d u a l b a c t e r i a o f the same o r d i f f e r e n t s p e c i e s (68). Possession of d e g r a d a t i v e p l a s m i d s a l l o w s microorganisms t o "experiment" w i t h a u x i l i a r y m e t a b o l i c pathways v i a gene m u t a t i o n o r p r o m i s c u o u s g e n e t i c exchange w i t h o u t j e o p a r d i z i n g t h e i r r e p l a c e a b l e genes on t h e c e n t r a l chromosome. The u l t i m a t e s e l e c t i v e f a c t o r i n d e t e r m i n i n g whether a n o v e l o r g a n i c compound c a n p r o v i d e the s e l e c t i v e advantage n e c e s s a r y to i n d u c e c a t a b o l i c a d a p t a t i o n appears t o be i t s a b i l i t y t o s u p p o r t the s y n t h e s i s o f a t l e a s t one m o l e c u l e o f ATP d u r i n g i t s d e g r a d a t i o n (5,48). As Delwiche has o b s e r v e d "Few e n e r g y - y i e l d i n g r e a c t i o n s have not been e x p l o i t e d by microorganisms, and some f o r m i d a b l e o b s t a c l e s to e x p l o i t a t i o n have been overcome by i n g e n i o u s a d a p t a t i o n s , some o f which r e m a i n t o be e x p l a i n e d by the m i c r o b i o l o g i s t " ( 5 ) . Enhanced P e s t i c i d e

Biodegradation

In l i g h t o f the m e t a b o l i c a d a p t a b i l i t y o f m i c r o o r g a n i s m s r e s i d i n g i n t h e e n e r g y - p o o r environment o f the s o i l , i t s h o u l d not t h e n be s u r p r i s i n g t h a t s o i l - a p p l i e d p e s t i c i d e s c a n be degraded b i o l o g i c a l l y and t h a t m i c r o b i a l a d a p t a t i o n f o r p e s t i c i d e c a t a b o l i s m would be possible. T h i s f a c t became apparent not l o n g a f t e r t h e i n t r o d u c t i o n of the f i r s t s y n t h e t i c o r g a n i c p e s t i c i d e s (e.g., phenoxyacetic a c i d herbicides). V e r y e a r l y work d e m o n s t r a t e d t h a t 2,4-D d i s s i p a t e d much more s l o w l y from a u t o c l a v e d ( i . e . , s t e r i l i z e d ) s o i l t h a n from n a t u r a l s o i l (69). I n t r i g u e d by the p o s s i b i l i t y o f m i c r o b i a l d e g r a d a t i o n , L . J . Audus o f t h e Botany Department o f B e d f o r d C o l l e g e U n i v e r s i t y , London, began a s e r i e s o f i n v e s t i g a t i o n s t h a t f i r s t c l e a r l y e l u c i d a t e d the r o l e o f s o i l m i c r o o r g a n i s m s i n t h e d e g r a d a t i o n o f p e s t i c i d e s a p p l i e d to s o i l . In h i s e x p e r i m e n t s Audus r e c y c l e d an aqueous s o l u t i o n o f 2,4-D (10-1,000 fxg/ml) t h r o u g h a column packed with garden s o i l . U s i n g b i o a s s a y t e c h n i q u e s he was a b l e t o demonstrate that a f t e r a d e f i n e d l a g p e r i o d , d u r i n g which l i t t l e 2,4-D d e g r a d a t i o n was noted, t h e r e f o l l o w e d a p e r i o d o f v e r y r a p i d p e s t i c i d e d e g r a d a t i o n t o n e g l i g i b l e l e v e l s (31). A s e c o n d key f i n d i n g o f t h i s s t u d y was t h a t a second dose o f 2,4-D r e c y c l e d t h r o u g h t h e s o i l column was i m m e d i a t e l y degraded w i t h no l a g p e r i o d evident. These s o i l p e r f u s i o n s t u d i e s were q u i c k l y f o l l o w e d by o t h e r i n v e s t i g a t i o n s which d e m o n s t r a t e d t h a t s o i l p r e t r e a t e d w i t h 2,4-D d i s p l a y e d t h e a b i l i t y t o more r a p i d l y degrade a subsequent dose o f 2,4-D t h a n p r e v i o u s l y u n t r e a t e d s o i l (70). The m i c r o b i a l l y - m e d i a t e d n a t u r e o f t h i s p r o c e s s was l a t e r c o n f i r m e d t h r o u g h t h e i s o l a t i o n o f 2,4-D c a t a b o l i z i n g m i c r o o r g a n i s m s and the s t u d y o f 2,4-D degrading p o p u l a t i o n s o f s o i l microorganisms (71-74). D u r i n g the 30 y e a r s f o l l o w i n g the d i s c o v e r y o f m i c r o b i a l a d a p t a t i o n f o r p e s t i c i d e d e g r a d a t i o n , t h e r e were i n t e r m i t t e n t r e p o r t s o f t h e same phenomenon a f f e c t i n g t h e p e r s i s t e n c e o f o t h e r p e s t i c i d e s . However, due t o t h e f a c t t h a t v i r t u a l l y none o f t h e s e r e p o r t s c o n c e r n e d s i t u a t i o n s where r e d u c e d p e s t i c i d e p e r s i s t e n c e a f f e c t e d pest c o n t r o l e f f i c a c y , m i c r o b i a l adaptation f o r p e s t i c i d e degradation was l a r g e l y r e l e g a t e d t o the s t a t u s o f academic c u r i o s i t y . In f a c t ,



1.

RACKE


9

t h e f o c u s o f e n v i r o n m e n t a l c h e m i s t s d u r i n g much o f t h i s p e r i o d was on t h e r e c a l c i t r a n c e and lack o f d e g r a d a t i o n o f many e a r l y p e s t i c i d e s . By t h e mid 1970*s, t h e replacement o f t h e s e m a t e r i a l s w i t h d e g r a d a b l e , s o i l - a p p l i e d p e s t i c i d e s i n n e a r l y a l l markets s e t t h e scene f o r t h e development o f c u r r e n t i n t e r e s t i n a d a p t e d m i c r o b i a l p e s t i c i d e degradation. Although agronomists p e r i o d i c a l l y observe f a i l u r e s o f s o i l a p p l i e d p e s t i c i d e s t o c o n t r o l t a r g e t p e s t s , t h e s e have h i s t o r i c a l l y been a t t r i b u t e d t o improper a p p l i c a t i o n t e c h n i q u e , u n u s u a l e n v i r o n m e n t a l c o n d i t i o n s , o r development o f p e s t r e s i s t a n c e . However, a p a t t e r n o f p e s t c o n t r o l f a i l u r e s a f t e r a p p l i c a t i o n o f n o r m a l l y e f f i c a c i o u s s o i l p e s t i c i d e s emerged i n t h e l a t e 1970*s. In New Z e a l a n d , W i s c o n s i n , Nebraska, and Iowa the c a r b a m o t h i o a t e h e r b i c i d e EPTC no l o n g e r p r o v i d e d e f f e c t i v e c o n t r o l o f c e r t a i n weeds i n some f i e l d s w i t h h i s t o r i c use o f EPTC (75-78). In I l l i n o i s , Iowa, Kansas, and E a s t e r n Canada the carbamate i n s e c t i c i d e c a r b o f u r a n d i d not p r o v i d e adequate p r o t e c t i o n a g a i n s t c e r t a i n s o i l i n s e c t p e s t s i n some s o i l s w i t h h i s t o r i c c a r b o f u r a n use (79-83). The f a i l u r e s o f t h e s e and a few o t h e r p e s t i c i d e s were e v e n t u a l l y r e c o g n i z e d t o o c c u r due t o r a p i d m i c r o b i a l d e g r a d a t i o n t h a t m a n i f e s t e d i t s e l f a f t e r a p a r t i c u l a r p e s t i c i d e had been a p p l i e d f o r two o r more c o n s e c u t i v e y e a r s t o the same f i e l d . T h i s phenomenon came t o be termed "enhanced d e g r a d a t i o n " o r " a c c e l e r a t e d d e g r a d a t i o n " , because a more r a p i d r a t e o f p e s t i c i d e d e g r a d a t i o n was o b s e r v e d i n p r e v i o u s l y t r e a t e d t h a n i n previously untreated f i e l d s . The term "enhanced d e g r a d a t i o n " has come t o be synonymous w i t h adapted m i c r o b i a l c a t a b o l i s m . S i n c e enhanced d e g r a d a t i o n has come t o the f o r e f r o n t o f e n v i r o n m e n t a l c h e m i s t r y , much r e s e a r c h e f f o r t has been d i r e c t e d a t u n d e r s t a n d i n g t h e f i e l d i m p l i c a t i o n s , m i c r o b i o l o g y , and b i o c h e m i s t r y o f t h i s phenomenon. The c h a p t e r s which f o l l o w i n t h i s book have been o r g a n i z e d so as t o convey the d e p t h o f u n d e r s t a n d i n g we have a c h i e v e d regarding microbial adaptation f o r p e s t i c i d e degradation. These c h a p t e r s r e v e a l t h a t we s h o u l d not o n l y v i e w t h i s phenomenon as an a g r i c u l t u r a l problem r e q u i r i n g management and s o l u t i o n s , but as a window i n t o t h e remarkable a d a p t a b i l i t y and c o m p l e x i t y o f t h e s o i l m i c r o b i a l ecosystem.

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