Glutathione Conjugation and Contaminant Transformation

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Critical Review

Glutathione Conjugation and Contaminant Transformation JENNIFER A. FIELD* Department of Agricultural Chemistry, Oregon State University, Corvallis, Oregon 97331

E. M. THURMAN U.S. Geological Survey. Lawrence, Kansas 66049

The recent identification of a novel sulfonated metabolite of alachlor in groundwater and metolachlor in soil is likely the result of glutathione conjugation. Glutathione conjugation is an important biochemical reaction that leads, in the case of alachlor, to the formation of a rather difficult to detect, water-soluble, and therefore highly mobile, sulfonated metabolite. Research from weed science, toxicology, and biochemistry is discussed to support the hypothesis that glutathione conjugation is a potentially important detoxification pathway carried out by aquatic and terrestrial plants and soil microorganisms. A brief review of the biochemical basis for glutathione conjugation is presented. We recommend that multidisciplinary research focus on the occurrence and expression of glutathione and its attendant enzymes in plants and microorganisms, relationships between electrophilic substrate structure and enzyme activity, and the potential exploitation of plants and microorganisms that are competent in glutathione conjugation for phytoremediation and bioremediation.

Introduction Recent interest and successes in phytoremediation and bioremediation obviate the need for an improved understanding of enzyme-mediated transformation of contaminants in terrestrial and aquatic environments (1, 2). Research on the occurrence, reactivity, and specificity of enzymes is attracting attention in an effort to understand and ultimately control biochemical reactions that are useful for the remediation of contaminated soil and water. Of the myriad of enzymes present in biological systems, one challenge is to identify environmentally-relevant enzymes (2). The occurrence of contaminant metabolites in the environment provides important clues about the nature of * Corresponding author telephone: (503) 737-2265; fax: (503) 7370497; e-mail address: [email protected].

0013-936X/96/0930-1413$12.00/0

 1996 American Chemical Society

contaminant transformation pathways and their attendant enzymes. In particular, the identification of metabolites that contain atoms, such as sulfur, that are not found in the parent compound suggests rather specific transformation pathways. Enzymatically-mediated conjugation reactions between electrophilic contaminants and biological nucleophiles (thiols) result in the formation of unanticipated and difficult to detect metabolites. Conjugation reactions with glutathione have been suggested as an important pathway of contaminant transformation, particularly in the pesticide literature. Relatively little information is available on the extent to which glutathione conjugation in plants and microorganisms affect the mass balance of contaminants in the environment.

Aerobic Dechlorination Product: A Novel Sulfonated Metabolite Recently, a novel sulfonated metabolite (2-[(2,6-diethylphenyl)(methoxymethyl)amino]-2-oxoethanesulfonic acid) of the pre-emergent herbicide alachlor was detected in groundwater in several states in the Midwest (Figure 1) at concentrations ranging from 2 to 74 µg/L (3-5) and in surface water from 0.2 to 1.5 µg/L (6). In addition, a sulfonated metabolite of metolachlor was recently detected in soil (7). The sulfonated metabolite of alachlor is nonmutagenic and does not bioaccumulate, whereas alachlor is considered a potential human carcinogen (8). Unfortunately, no toxicity data are available on the previously unreported sulfonated metabolite of metolachlor. From a risk assessment point of view, the observation of the sulfonated metabolite of alachlor in groundwater is important because the sulfonated metabolite cross-reacts with antibodies raised against alachlor, thereby creating false positive reactions in immunoassay tests for the presence of alachlor in surface and groundwater (3, 9, 10). Central to the topic of this paper, the detection of a sulfonated metabolite of alachlor in groundwater is direct evidence that dechlorination reactions lead to the formation of sulfur-containing metabolites. The presence of a sulfur atom in the metabolite of alachlor clearly indicates a reaction involving a sulfur-bearing nucleophile. One recognized pathway for incorporating sulfur is through conjugation reactions involving the addition or displace-

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FIGURE 1. Map of midwestern United States indicating detection of alachlor and its sulfonated metabolite.

ment of an electrophilic functional group, such as chlorine, by a nucleophilic thiol group. Conjugation reactions between electrophilic compounds and glutathione, a biological thiol compound, is a detoxification reaction common in the defense of mammals, fish, insects, higher plants, and microorganisms against oxidative stress (11-16). Glutathione conjugation detoxifies a broad spectrum of electrophilic compounds used in agriculture and industry including alkylhalides (17, 18), triazine herbicides (13), chlorobenzenes (19), organophosphorous insecticides (20), nitroaromatic compounds (21), chloroacetanilide herbicides (22, 23), sulfonyl urea herbicides (24), diphenyl ether herbicides (25-27), polyaromatic hydrocarbons (28), pyrrolizidine alkaloids (29), and hydroquinones (30). Glutathione has been implicated in the dechlorination of common industrial pollutants, including dichloromethane and pentachlorophenol (1, 31); however, in these two cases, glutathione is used catalytically in carbon metabolism so that conjugates are not formed. In addition, some compounds are bioactivated to toxic, mutagenic, or carcinogenic forms upon conjugation with glutathione, including vicinal halogenoalkanes (e.g., 1,2-dibromoethane), haloalkenes (e.g, hexachlorobutadiene), bromohydroquinones, and isothiocyanate (32-34). While glutathione and its attendant enzymes are widely recognized by biochemists, toxicologists, and weed scientists (35-40), this enzyme-mediated reaction, which occurs both in plants and soils, has received little attention from environmental chemists, microbiologists, and engineers. While not all reactions with glutathione lead to the formation of conjugates, those that do form conjugates and sulfonated metabolites have significant environmental implications. The extremely low pKa of sulfonic acids means that the functional group is ionized at the pH of most environmental systems. Therefore, the sulfonic acid group

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imparts a degree of water solubility to molecules so that the mobility of sulfonated metabolites is enhanced over that of the parent compound. Detection of the sulfonated metabolite in groundwater attests to the mobility and potential persistence of sulfonated compounds. Incidentally, the identification of a water-soluble metabolite of a chloroacetanilide herbicide has potential economic ramifications because the registration of acetochlor, a recently registered chloroacetanilide herbicide, contains a revocation clause should residues be found to leach into groundwater (41). Because sulfonated metabolites were not initially anticipated, identification of the metabolite required analytical detective work. The metabolite gave a false positive in an alachlor immunoassay yet was not detected by gas chromatography/mass spectrometry. The indirect route leading to the identification of the sulfonated metabolite underscores the difficulty in detecting sulfonated compounds in the environment. Sulfonated compounds are rather difficult to detect analytically because sulfonates typically exhibit low volatilities that impede their analysis by gas chromatography/mass spectrometry. An elaborate isolation scheme and pyrolysis mass spectrometry was used by van Loon et al. (42) to identify a large pool of sulfonated compounds in the Rhine River that had gone previously undetected. Because of the difficulty in sulfonated compound detection, sulfur-incorporating reactions may be overlooked as a set of environmentally relevant transformation reactions simply because some of the major metabolites are not readily detected by conventional analytical procedures. In addition to the fact that relatively little information is available on the formation of sulfonates, a rather limited number of degradation pathways are described for naturallyoccurring and xenobiotic sulfonated compounds. Naturally

occurring aliphatic sulfonates, including taurine, cysteic acid, and methanesulfonic acid, are desulfonated by soil bacteria (43, 44). The most commonly described pathway for the aerobic desulfonation of aromatic sulfonates is attack by dioxygenases to form the corresponding catechol followed by ring cleavage (45, 46). The biodegradation of aromatic sulfonates appears limited under anaerobic conditions as indicated by the persistence of sulfonated compounds in anaerobic groundwater and sewage sludge digestors (43, 47, 48). In addition to their utilization as carbon and energy sources, sulfonated compounds potentially can be utilized as sole sulfur sources. A wide range of aliphatic and aromatic sulfonates, including the sulfonated metabolite of metazachlor, are utilized by bacteria as sole sulfur sources (49-54). However, the presence of sulfate limits the use of sulfonates as sole sulfur sources so that sulfonate utilization may occur only under nutrient-limiting conditions (49, 52, 53). Additional research is required to determine the significance of sulfonate utilization as a sole sulfur source under environmental conditions. This critical review provides an overview of selected literature from the fields of biochemistry, microbiology, toxicology, and weed science to argue that glutathione is ubiquitous and an potentially important biochemical in the fate and transformation of electrophilic pollutants, especially chlorinated pollutants. The focus of this review is on the transformation of electrophilic compounds by glutathione conjugation and is not intended to serve as a review of dechlorination reactions nor of bioremediation as several excellent reviews exist (55, 56). Rather, this review is intended to bring attention to novel sulfonated metabolites of pesticides that illustrate the potential environmental relevance of glutathione conjugation. Electrophilic contaminant transformation by glutathione conjugation is a potentially significant, yet overlooked, detoxification pathway that occurs in indigenous plants and microorganisms in aquatic and terrestrial environments.

Glutathione Conjugation Glutathione [N-(N-L-glutamyl-L-cysteinyl)glycine], an ubiquitous tripeptide, plays an important detoxification role through its reaction with electrophilic xenobiotic compounds to form typically less toxic, water-soluble, and excretable products. Several excellent reviews exist on the evolution and function of glutathione and its attendant enzymes in maintaining the redox status in cells (35, 57). For example, glutathione acts an antioxidant to prevent cellular damage by maintaining essential thiols (RSSR) (e.g., cysteine and coenzyme A) in their reduced state (RSH) (eq 1), scavenging hydrogen peroxide (eq 2), and hydroxyl radicals (eq 3) (57-59).

FIGURE 2. Glutathione S-transferase enzyme-mediated reaction between glutathione and the chloroacetanilide herbicide alachlor to form sulfonated and non-sulfonated metabolites.

to organism resistance and adaptation to a variety of physical and chemical stresses encountered in the environment (58, 59). Elevated levels of glutathione and glutathione reductase have been observed in plants exposed to stresses such as heat (60), cold and salinity (61, 62), air pollutants including ozone and sulfur dioxide (63-65) and heavy metals (66-68). Glutathione plays a critical role in the mercapturic acid biosynthesis pathway in which electrophilic compounds are conjugated to form S-substituted N-acetyl cysteines (35). The initial steps in metabolism proceed via a sequential removal of chlorine through an enzyme-mediated reaction with glutathione (Figure 2). Subsequently, γ-glutamic acid is removed by a γ-glutamyltranspeptidase, and the glycine moiety then is cleaved by one or more carboxypeptidases. Cysteine β-lyases are responsible for the cleavage of the sulfur-carbon bond of the cysteinyl moiety. In plants and mammals, a variety of reduced and partially oxidized sulfur-containing metabolites (e.g., methylthio, methylsulfinyl, methylsulfonyl) are formed as a consequence of glutathione conjugation with chloroacetanilide herbicides (23, 69). More oxidized forms of sulfurand non-sulfur-containing metabolites (e.g., sulfonate, sulfinylacetic, and oxalic acid) are observed for microbiallyactive soils (Figure 2) (70, 71).

2GSH + RSSR S GSSG + 2RSH

(1)

2GSH + H2O2 S GSSG + 2H2O

(2)

GSH + HO• f GS• + H2O

Glutathione Conjugation in Aquatic and Terrestrial Environments

(3)

Plants. Glutathione conjugation plays a major role in plant resistance to herbicides (38, 72-76). The glutathione S-transferase enzyme-mediated reactions involving glutathione are some of the principal detoxification pathways for crop resistance to herbicides (Table 1). For example, corn, soybean, peanut, and sorghum resistance to diphenyl ether, triazine, and chloroacetanilide herbicides are based on the glutathione conjugation detoxification pathway (23,

Glutathione reactions with electrophilic chemicals are catalyzed by glutathione S-transferase enzymes. Glutathione S-transferase enzymes are present in most organisms, including plants, animals, protozoa, fungi, and bacteria (13). Increases in glutathione, glutathione reductase, and glutathione S-transferase levels have been linked

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TABLE 1

Plants That Resist Damage by Herbicides through Glutathione Conjugation plant corn (Zea mays L.) soybean (Glycine max L.) soybean (Glycine max L.) sorghum (Sorghum bicolor) peanut (Arachis hypogaea L. Cv. Spanish) corn spruce (Picea abies L. Karst) cotton (Gossypium hirsutum L.)

pesticide

ref

atrazine 38, 77, 104 propachlor 23 acifluorfen 25 metolachlor 15 pentachloronitro- 105, 106 benzene EPTC 73, 107 fluorodifen 26, 27 paraquat 58

25, 77). The level of plant tolerance or susceptibility to herbicides is affected by the glutathione S-transferase enzyme content and activity as well as the structure of the herbicide (75). Unfortunately, what little information exists on the structure-reactivity relationship between glutathione and electrophilic chemicals is largely limited to chloroacetanilide herbicides in crops (74, 75). An increasing number of reports provide evidence that plant rhizospheres promote chemical degradation; however, little information is currently available on the pathways and mechanisms of electrophilic chemical transformation in the rhizosphere. Because plants may accelerate the removal of contaminants, the chemical form and quantity of residues, particularly water-soluble sulfonates, released during the life cycle of the plant needs to be better understood. Because thioanisoles, thioethers, sulfoxides, and sulfones have been detected as pesticide metabolites in crops (23, 71, 37), plants represent potential sources of xenobiotic sulfur-containing metabolites in aquatic and terrestrial environments. Lamoreaux and Rusness (23) found that propachlor detoxification in hydroponically-grown soybeans did not result in the formation of sulfonated metabolites. Rather, they detected glutathione conjugates and conjugate cleavage products in soybeans containing more reduced forms of sulfur. In contrast, they detected more oxidized metabolites, including sulfonate and sulfinylacetic metabolites, in soil without soybeans and in soil-grown soybeans, suggesting that the highly oxidized sulfur-containing metabolites first are formed in soil and subsequently taken up by soybean plants. Additional research is needed to confirm if sulfur-containing metabolites are transferred between plants and soils and to determine the degree to which plants and soil microorganisms contribute to the pool of sulfur- and nonsulfur-containing metabolites observed in the terrestrial environment. Algae. In addition to higher plants, algae conjugate electrophilic compounds with glutathione. Specific glutathione S-transferase enzymes have been identified and characterized in algae (82). Lamoreaux and Rusness (37) demonstrated that the algae Gleotrichia echinulata in lake water metabolized pentachloronitrobenzene by glutathione conjugation. An aquatic plant, Eichhornia crassipes, which is commonly used in wastewater treatment plants, was shown by Roy and Ha¨nninen (78) to produce dechlorinated metabolites and bound conjugates of pentachlorophenol. Plant enzymes may become useful biomarkers of plant exposure to pollutants because increases in glutathione content and in glutathione S-transferase activity in aquatic plants and macrophytes indicate exposure to electrophilic compounds (78-81). More research is required to un-

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derstand the importance of glutathione conjugation on the transformation of electrophilic chemicals in natural aquatic environments as well as in municipal and industrial wastewater treatment plants. Terrestrial Microorganisms. Several species of fungi, protozoa, and bacteria contain glutathione S-transferase enzymes (82-85). Of the microorganisms tested, protozoa have the highest glutathione S-transferase activity followed by fungi and bacteria. Fungi metabolize pentachloronitrobenzene, dichloronitrobenzene, and chloronitrobenzene by means of glutathione conjugation (86-88). Others have reported transformations of alachlor and metolachlor to sulfur-containing metabolites by a consortia of microorganisms, although glutathione conjugation was not specifically implicated (89-92). Feng (71) demonstrated that acetochlor and the glutathione conjugate of acetochlor both degrade in soil to sulfonate, sulfinylacetic, and oxanilic acid metabolites, suggesting that acetochlor transformation in soil occurs through glutathione conjugation. With the use of selective inhibitors, Feng (71) established that the degradation of the acetochlor-glutathione conjugate was blocked by the addition of a γ-glutamyl transpeptidase inhibitor. In addition to γ-glutamyl transpeptidase, the enzyme cysteine β-lyase occurs in soil bacteria and is responsible for the degradation of the glutathione conjugate to sulfur-containing metabolites (71, 85, 93). Soil bacterial monooxygenases have been shown to attack thiols and thioethers to form sulfoxides (94). The presence of glutathione and glutathione S-transferase enzymes in microorganisms suggests that the transformation of electrophilic chemicals by glutathione conjugation may commonly occur in natural waters and in terrestrial environments. In our laboratories, we have shown that the transformation of alachlor to the sulfonic acid metabolite in agricultural top soil is a biological process that occurs under aerobic conditions. Abiotic reactions between glutathione and electrophilic compounds are likely limited to reducing environments, such as marine sediments where free glutathione occurs and is considered a component of the biogeochemical sulfur cycle (95-97). The reactivity of glutathione as a nucleophile with a thiol group with a pKa of 8.6 (35, 98) is expected to be rather slow in oxic aqueous environments at near-neutral pH (99). In the quest to identify and manipulate enzymes and the genes that encode the enzymes for use in phytoremediation and bioremediation (1, 2), glutathione and its associated enzymes should not be overlooked. Characterization of the GST genes in indigenous microorganisms and subsequent development of gene probes would make it possible to screen numerous soil bacteria. Gene sequences are described for two glutathione S-transferase enzymes involved in the transformation of industrial pollutants, including dichloromethane dehalogenase from Methylobacterium (18) and pentachlorophenol dehalogenase from Flavobacterium (31). Additionally, a GST gene was identified in the Pseudomonas strain LB400 that is capable of degrading polychlorinated biphenyls (100). Although the function of the gene is not known; it is thought to be involved in the dehalogenation of PCB degradation products. While the gene shows some similarity to that of the Flavobacterium, further research is required to establish the degree of homology. Research is needed to characterize additional GST genes in indigenous soil bacteria that are competent in glutathione conjugation. Gene insertion is

one potential strategy for use in bioremediation as GST genes from maize already have been successfully inserted into Escherichia coli where the activity of the enzyme was expressed as the ability of the bacterial extracts to conjugate atrazine (101) and alachlor (102).

Recommendations Field observations of a novel sulfonated metabolite of alachlor in groundwater and surface water clearly indicate the environmental significance of biochemical sulfurincorporating reactions. Literature on glutathione conjugation from the disciplines of weed science, biochemistry, toxicology, microbiology, and molecular biology provide a compelling argument for the ubiquity of glutathione and its potential role in the detoxification of contaminants in aquatic and terrestrial environments. Because glutathione conjugation is a potentially important environmental phenomena involving multiple organisms, it is worthy of more attention from environmental scientists. Multidisciplinary research is required to elucidate fundamental relationships between the distribution of organisms competent in glutathione conjugation and electrophilic contaminant transformation. Structurereactivity relationships should be explored in order to better understand the selectivity of GST enzymes and to predict whether contaminants will form conjugates with glutathione or use glutathione as a catalyst. Even though GST enzymes occur in many soil bacteria, little is known of their properties and of the genes that encode them. Research is needed to determine how widely various GST genes are distributed within indigenous microbial communities and their level of expression. Research is required to understand the occurrence and expression of glutathione and GST enzymes in indigenous plants and microorganisms as indigenous species are believed to be the most promising and economically feasible for implementation in phytoremediation and bioremediation strategies (103). Understanding the environmental relevance and dynamics of glutathione conjugation will contribute toward the exploitation of organisms for the phytoremediation and bioremediation of contaminated soils and water.

Acknowledgments This is Technical Report 10,924 of the Oregon Agricultural Experiment Station.

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Received for review April 26, 1995. Revised manuscript received January 19, 1996. Accepted February 12, 1996.X ES950287D X

Abstract published in Advance ACS Abstracts, March 15, 1996.