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Environmental Chemistry MICROBIAL TRANSFORMATION of PYRETHROID INSECTICIDES in AQUEOUS and SEDIMENT PHASES

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Environmental Chemistry MICROBIAL TRANSFORMATION of PYRETHROID INSECTICIDES in AQUEOUS and SEDIMENT PHASES Environmental Toxicology and Chemistry, Vol. 23, No. 1, pp. 1±6, 2004 q 2004 SETAC Printed in the USA 0730-7268/04 $12.00 1 .00 Environmental Chemistry MICROBIAL TRANSFORMATION OF PYRETHROID INSECTICIDES IN AQUEOUS AND SEDIMENT PHASES SANGJIN LEE,² JIANYING GAN,*² JONG-SIK KIM,² JOHN N. KABASHIMA,³ and DAVID E. CROWLEY² ²Department of Environmental Sciences, University of California±Riverside, Riverside, California 92521, USA ³University of California South Coast Research and Extension Center, Irvine, California 92618, USA (Received 21 February 2003; Accepted 28 April 2003) AbstractÐRecent studies showed that synthetic pyrethroids (SPs) can move via surface runoff into aquatic systems. Fifty-six of SP-degrading bacteria strains were isolated from contaminated sediments, of which six were evaluated for their ability to transform bifenthrin and permethrin in the aqueous phase and bifenthrin in the sediment phase. In the aqueous phase, bifenthrin was rapidly degraded by strains of Stenotrophomonas acidaminiphila, and the half-life (t1/2) was reduced from .700 h to 30 to 131 h. Permethrin isomers were degraded by Aeromonas sobria, Erwinia carotovora, and Yersinia frederiksenii. Similar to bifenthrin, the t1/2 of cis- and trans-permethrin was reduced by approximately 10-fold after bacteria inoculation. However, bifenthrin degradation by S. acidaminiphila was signi®cantly inhibited in the presence of sediment, and the effect was likely caused by strong adsorption to the solid phase. Bifenthrin t1/2 was 343 to 466 h for a ®eld sediment, and increased to 980 to 1200 h for a creek sediment. Bifenthrin degradation in the inoculated slurry treatments was not greatly enhanced when compared with the noninoculated system. Therefore, although SP-degrading bacteria may be widespread in aquatic systems, adsorption to sediment could render SPs unavailable to the degraders, thus prolonging their persistence. KeywordsÐBifenthrin Permethrin Bioavailability Adsorption Biodegradation INTRODUCTION ments, partitioning into the solid phase could have a profound effect on the transformation rate and hence the persistence of Synthetic pyrethroids (SPs) have been widely used for in- SPs. sect control on agricultural crops, animals, and in households. The main objectives of this study were to identify SP-de- The use of SPs in the United States may increase sharply as grading bacteria from previously contaminated sediments and organophosphate products such as diazinon and chlorpyrifos to compare the degradability of SPs by bacterial isolates in are being phased out for certain uses. Synthetic pyrethroids aqueous systems (BF and PM) and in sediment phases (BF). generally have little or no mammalian toxicity but are effective for controlling many insects when used at low rates [1]. Al- Bifenthrin is a relatively new SP and is characterized by greater though SPs are known for their poor mobility in soil after photostability and insecticidal activity than previous SPs [5,6], application, recent studies have shown that surface runoff may and PM is currently the most widely used SP. Runoff of both transport particle-associated SPs to surface water [2±4]. pesticides to rivers and creeks has been observed in certain Pyrethroids commonly have high acute toxicity to ®sh and watersheds [2,4]. aquatic invertebrates. For instance, the 50% lethal concentra- tion (LC50) of bifenthrin (BF) is 0.07 mg/L for Ceriodaphnia MATERIALS AND METHODS dubia and 0.15 mg/L for rainbow trout [5,6], while the re- Chemicals and sediments spective values for permethrin (PM) are 0.55 and 9.0 mg/L [5,6]. Once in natural water systems, pyrethroids tend to dis- Standards of Z-(cis)-bifenthrin (.98% purity) and per- appear quickly from the water column due to their strong methrin (20% cis and 78% trans) were purchased from Chem af®nity for sediment [1]. Therefore, the overall risk of SPs in Service (West Chester, PA, USA). Organic solvents used for aquatic systems depends closely on their persistence in the extraction were of pesticide residue or high-pressure liquid sediment phase, which in turn is determined by their suscep- chromatography grade. tibility to microbial degradation. Knowledge of microbial deg- A previously contaminated sediment was obtained from a radation rates should also indicate if bioremediation would be runoff channel at a nursery site in Orange County (CA, USA) feasible for SP-contaminated sediment or water. However, mi- and used for enriching SP-degrading bacteria. Products of BF crobial degradation of SPs has been studied only to a limited and PM had been used at the nursery for over three years prior extent. While earlier studies did show that SP degradation in to the sampling. The moist sediment was stored at 48C before soils was attributable to microbial activity [7±9], only a few use. Two SP-free sediments were collected in the Newport Bay studies attempted to identify SP-degrading bacteria, and soil Watershed in Orange County for use in the biodegradation was the only medium tested [8±11]. Subsequent biodegrada- experiments. A ®eld sediment was taken from a drainage chan- tion was demonstrated only in solid-free microbial cultures nel in an agricultural ®eld, and a creek sediment was collected [9±11]. Because surface waterbodies always contain sedi- from the San Diego Creek near Irvine, California. These sed- iments were air dried for 48 h and passed through a 0.5-mm * To whom correspondence may be addressed sieve before use. The ®eld sediment contained 86% sand, 7% ([email protected]). silt, 7% clay, and 0.13% organic carbon. The creek sediment 1 2 Environ. Toxicol. Chem. 23, 2004 S. Lee et al. contained 76% sand, 15% silt, 9% clay, and 1.04% organic (BF) or 0.2 mg/ml (PM). Twenty milliliters of the spiked so- carbon. lution were transferred to 40-ml screw-top vials. For BF, each vial was inoculated with one of the three strains at 6.5 3 107 SP-degrading bacteria isolation to 3.4 3 108 colony-forming units (CFUs). For PM, vials were Approximately 10 g of the SP-contaminated sediment was inoculated with one of the three selected isolates at 1.8 to 2.6 mixed in 100 ml of mineral salt (MS) medium in a 250-ml 3 107 CFUs. All treatments were incubated at room temper- ¯ask, and 10 ml of 1.0 mg/ml BF or PM solution (acetone) ature on a platform shaker. At different time intervals, triplicate were added. The MS medium was made by dissolving 0.5 g samples were removed for analyzing SP concentrations. The K2HPO4, 0. 5 g NaNO3, 0.2 g MgSO4´7H2O, trace FeSO4´7H2O, sample was transferred to a 250-ml separatory funnel and ex- and 15 g agar in 1,000 ml distilled water. The ¯asks were tracted twice with 50 ml of ethyl acetate. The ethyl acetate incubated on a platform shaker at room temperature. After 2 extracts from the same samples were combined, dried with 5 weeks, a 5.0-ml aliquot of the aqueous fraction was removed g of anhydrous sodium sulfate, and then concentrated to near from the culture and transferred to a new ¯ask containing 100 dryness on a rotary evaporator at 608C. The residues were ml fresh MS medium, and was treated with a fresh spike of recovered in 5.0 ml of hexane-acetone (1:1 v/v), and then BF or PM. The same enrichment step was repeated for a total analyzed by GC. Preliminary experiments showed that the of three times. The bacterial growth was monitored by ob- recovery of BF or PM for the above extraction and analysis serving turbidity on a spectrophotometer (Beckman DU 640; procedures was .90%. Beckman, Fullerton, CA, USA). After serial dilution, 100 ml An Agilent 6890N GC system with electron capture detec- of solution was removed and spread onto triplicate plates that tor (Agilent, Wilmington, DE, USA) was used for analysis of were incubated for 10 d at 288C. BF and PM. An Agilent-5 capillary column (30 m 3 0.32 mm 3 0.25 mm) was used for separation, with helium as the carrier Identi®cation of SP-degrading bacteria isolates gas at 2.1 ml/min. The other GC parameters were as follows: The agar plate was divided into four quadrants, and 28 Inlet temperature, 2508C; detector temperature, 3008C; oven bacterial colonies from one quadrant were subjected to iden- temperature, initially 1508C for 1.0 min, ramped to 2808Cat ti®cation using the MIDI (Microbial ID, Newark, DE, USA) 158C/min, and kept at 2808C for 5.0 min; and injection volume, fatty acid methyl ester system [12]. The isolates were streaked 1.0 ml. Samples were introduced in the splitless mode. on trypticase soy-broth agar in four quadrants, and the plates were incubated at 288C for 24 h. A loopful of cell material of Biodegradation experiments in sediment slurry late log-phase cells was harvested. Fatty acids were extracted Degradation of BF by the three selected strains was further and methylated according to the procedures given by the man- compared between aqueous systems in the presence or absence ufacturer. Samples were analyzed on a Hewlett-Packard 6890 of a sediment solid phase. Two grams of the ®eld sediment or gas chromatography (GC) (Palo Alto, CA, USA) and were creek sediment were added into 40-ml vials containing 20 ml identi®ed using the MIDI microbial identi®cation software. of MS solution and 10.0 mg of BF. Bacterial strains were Three of the fastest growing bacteria isolates were selected inoculated into each treatment at a level similar to that used after BF or PM enrichment and were further subjected to DNA in the aqueous phase experiments. The spiked vials were in- sequence analysis [13,14]. The same strains were subsequently cubated on a platform shaker at room temperature.
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