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Hoaglandetal98jafc46.Pdf J. Agric. Food Chem. 1998, 46, 4759−4765 4759 Biotransformations of Fenoxaprop-ethyl by Fluorescent Pseudomonas Strains Robert E. Hoagland* and Robert M. Zablotowicz Southern Weed Science Research Unit, Agricultural Research Service, U.S. Department of Agriculture, P.O. Box 350, Stoneville, Mississippi 38776 Fenoxaprop-ethyl (FE) transformation by pure cultures of four Pseudomonas strains was studied using14C-labeled herbicide, labeled in either the dioxyphenyl (DOP) or the chlorophenyl (CP) ring. Resting cells rapidly hydrolyzed FE to fenoxaprop acid (FA), but cleavage of the ether bond proceeded slowly. Degradation of FE by P. fluorescens strains RA-2 and UA5-40 cultured in tryptic soy broth (TSB) or minimal media with glucose (MMG) or propionate (MMP) was assessed. TSB cultures completely hydrolyzed FE to FA within 5 days. Polar metabolites (predominantly glycylcysteine and cysteine conjugates arising from FE or FA), an unidentified metabolite, and 6-chloro- 2,3-dihydrobenzoxazol-2-one (CDHB) accumulated in TSB cultures treated with 14C-CP-labeled FE during an 11-day study, whereas 2-(4-hydroxyphenoxy)propionic acid accumulated in 14C-DOP- labeled FE-TSB cultures. FE transformation by MMP cultures was limited to ester hydrolysis of FE to FA. Hydrolysis of FE to FA was never detected in RA-2 MMG cultures and was low in UA5- 40 MMG cultures. Cleavage of the benzoxazolyloxyphenyl ether bond occurred in MMG cultures of both strains; that is, 50% of 14C-CP-labeled FE was recovered as CDHB, and hydroquinone 14 accumulated in MMG C-DOP-labeled FE cultures. No mineralization of FE to CO2 was observed, regardless of the 14C label or growth media used as substrate. Strains of P. fluorescens can promote significant cometabolic transformations of FE and may contribute to the dissipation of FE in the environment. Keywords: Herbicide; biodegradation; pseudomonad; microbial metabolism; aryloxyphenoxy propionate INTRODUCTION Studies using a mixed microbial consortium showed that ( FE can be utilized as a sole carbon and nitrogen source Fenoxaprop-ethyl [( )-ethyl 2-[4-[(6-chloro-2-benzox- (Gennari et al., 1995). FA and CDHB were the metabo- azolyl)oxy]phenoxy]propanoate] (FE) is commonly used lites identified in these studies. Among bacteria, the for postemergence control of various annual grass weeds genus Pseudomonas has a wide spectrum of metabolic in soybeans, rice, wheat, and turf (WSSA, 1994). The and cometabolic transformation capability for various metabolism of FE in various plant species has been xenobiotics, including herbicides (Ha¨ggbloom, 1992; studied, and its degradation pathway is relatively well- Houghton and Shanley, 1994). Previous research from defined (Hall and Stephenson, 1995; Yaacoby et al., our laboratory has indicated the potential for cleavage 1991; Hoagland et al., 1996; Edwards and Cole, 1996). of the ether linkage of the diphenyl ether herbicides Also, the fate of FE has been studied in soils from fluorodifen [2,4′-dinitro-4-(trifluoromethyl)diphenyl ether] several geographical areas (Ko¨cher et al., 1982; Smith (Zablotowicz et al., 1994) and acifluorfen [5-[2-chloro- and Aubin, 1990; Toole and Crosby, 1989). In these 4-(trifluoromethyl)phenoxy]-2-nitrobenzoic acid] (Zablo- studies, FE was rapidly hydrolyzed to fenoxaprop-acid towicz et al., 1997) by strains of such bacteria. We (FA). This hydrolysis occurred more rapidly in moist hypothesized that glutathione conjugation might also nonsterile soils, suggesting microbial degradation (Ko¨ch- be a mechanism for bacterial transformation of FE, er et al., 1982; Smith and Aubin, 1990). The metabolite especially among fluorescent pseudomonads. Strains of FA is phytotoxic and can inhibit seed germination of P. fluorescens and P. putida also possess esterase various grass weeds (Bieringer et al., 1982). FA un- activity on diverse substrates, for example, p-nitro- dergoes further degradation in soils, forming metabo- phenyl butyrate and fluorescein diacetate (Zablotowicz lites such as 6-chloro-2,3-dihydrobenzoxazol-2-one et al., 1996). Our objectives in these studies were to (CDHB), 4-[(6-chloro-2-benzoxazolyl)oxy]phenetole, and evaluate pure cultures of fluorescent pseudomonad 4-[(6-chloro-2-benzoxazolyl)oxy]phenol (Smith, 1985). 14 strains and their cell-free enzyme preparations for Studies using C-labeled FE showed that some me- ability to degrade FE. We also sought to assess the tabolites are incorporated into soil organic matter and interaction of nutrition and growth status on FE trans- microbial biomass, with some mineralization to CO2 formation. (Ko¨cher et al., 1982; Smith and Aubin, 1990). FE is also subject to photodegradation yielding CDHB, 2-(4-hy- droxyphenoxy)propanoic acid (HPP), and ethyl 2-(4- MATERIALS AND METHODS hydroxyphenoxy)propanoate (Toole and Crosby, 1989). Bacterial Strains. P. fluorescens strains BD4-13, RA-2, Very limited information exists on specific microor- and UA5-40 and P. putida strain M-17 have been previously ganisms that are capable of transforming FE in soils. described (Zablotowicz et al., 1995; Hoagland and Zablotowicz, 10.1021/jf980637q This article not subject to U.S. Copyright. Published 1998 by the American Chemical Society Published on Web 10/24/1998 4760 J. Agric. Food Chem., Vol. 46, No. 11, 1998 Hoagland and Zablotowicz Table 1. Rf Values for FE and Metabolites in Five TLC Solvent Systems solvent systems (A) (B) (C) (D) toluene/ethyl acetate/ chloroform/ butanol/acetic butanone/acetic (E) acetic acid/water, methanol/water, acid/water, acid/water, benzene/acetone, compounda 50:50:1:0.5 (v/v/v/v) 65:25:1 (v/v/v) 12:3:5 (v/v/v) 10:1:1 (v/v/v) 10:1 (v/v) FE 0.94 0.98 0.98 0.97 0.89 FA 0.14 0.53 0.83 0.97 0.00 CDHB 0.55 0.98 0.93 0.93 0.48 HPP 0.14 0.24 0.81 ndb 0.09 HQ 0.68 0.86 nd nd nd CDHB-GSH 0.00 nd 0.39 0.08 0.00 CDHB-GlyCys 0.00 nd 0.51 0.39 nd CDHB-Cys 0.00 nd 0.69 0.62 nd a FE, fenoxaprop-ethyl; FA, fenoxaprop acid; CDHB, 6-chloro-2,3-dihydrobenzoxazol-2-one; HPP, 2-(4-hydroxyphenoxy)propionate; HQ, hydroquinone; CDHB-GSH, S-(6-chlorobenzoxazole-2-yl)glutathione; CDHB-GlyCys, S-(6-chlorobenzoxazole-2-yl)glycylcysteine; CDHB- Cys, S-(6-chlorobenzoxazole-2-yl)cysteine. b nd, not determined. 1995). These cultures were maintained as frozen glycerol and centrifugation (14000g, 10 min). Recovery and analysis of FE tryptic soy agar stocks. Prior to use in these experiments, and metabolites were achieved by RAD-TLC using a toluene/ subcultures of these stocks were assessed for purity on ethyl acetate/acetic acid/water (50:50:1:0.5, v/v/v/v) solvent selective media (Gould et al., 1985) and dilute tryptic soy agar. system (A) (Tal et al., 1993). An additional study was Chemicals. All chemicals and solvents were of analytical conducted with cell suspensions of UA5-40 incubated with grade or higher purity. FE, 14C-labeled dioxyphenyl, and either 9.0 or 45.0 µM 14C-CP-labeled FE (3.6 and 18.0 kBq chlorophenyl (sp. act. ) 997.2 and 1107 MBq g-1, respectively) mL-1). Cells were incubated as above for 92 h. Studies were were supplied by AgrEvo, Frankfurt, Germany. The high- also performed using crude cell-free extracts (CFE) of P. purity unlabeled metabolite standards of FA (HOE 088406), fluorescens strains RA-2 and UA5-40. CFEs were prepared CDHB (HOE 054014), and HPP (HOE 096918) were also from washed cells that were disrupted by sonication and from provided by AgrEvo. These products were used without which structural cell wall material had been removed by further purification. Glutathione (GSH), glycylcysteine (Gly- centrifugation (22000g, 20 min). This yielded extracts of ∼5 -1 Cys), cysteine (Cys), and equine glutathione S-transferase mg mL protein in 50 mM KPi. CFEs (400 µL) were treated (GST) were obtained from Sigma Chemical Co. (St. Louis, MO). with14C-CP labeled FE, 0.45 nmol with or without 1.0 µmol of -1 Conjugates derived from FE or FA [the GSH conjugate [S-(6- GSH (in KPi). Final concentrations of 4 mg mL protein, 9.0 chlorobenzoxazole-2-yl)glutathione ) CDHB-GSH], the Gly- µM FE, and 0 or 2 mM GSH in a final volume of 0.5 mL were Cys conjugate [S-(6-chlorobenzoxazole-2-yl)glycylcysteine ) incubated at 100 rpm at 30 °C. Aliquots were removed at 2.5 CDHB-GlyCys], and the Cys conjugate [S-(6-chlorobenzox- and 5 h, terminated (3 volumes of acetone), and analyzed using azole-2-yl)cysteine ) CDHB-Cys]] were produced via alkaline- the butanol/acetic acid/water (12:3:5, v/v/v) and butanone/acetic mediated synthesis as described elsewhere (Breaux et al., acid/water (10:1:1, v/v/v) solvent systems (C and D, respec- 1987). The glutathione conjugate was also synthesized enzy- tively), as well as solvent system A (see Table 1). matically using equine GST. Experiment II: Degradation of FE by P. fluorescens Analysis. Thin-layer chromatography (TLC) was used for Strains Grown under Various Nutrient Regimes. P. analysis of FE and metabolites. In TLC analysis, aliquots (10- fluorescens strains RA-2 and UA5-40 were evaluated for 50 µL) were mechanically spotted (40 °C) with a multispotter growth on potential metabolites of FE: CDHB, ethanol, HPP, (Analytical Instruments, Inc., Baltimore, MD) on silica gel HQ, and propionate (250 mg L-1) compared to unamended plates with fluorescent indicator (20 × 20 cm, 250 µm; Novick’s mineral salts buffer (Novick and Alexander, 1985). Whatman, Clifton, NJ). Plates were developed 10 cm in Erlenmeyer flasks (50 mL) containing 20 mL of media were several solvent systems using Camag twin-trough chambers inoculated with washed cell suspensions of these strains (300 (Camag Scientific Inc., Wilmington, NC).
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