Transformation of Chiral Polychlorinated Biphenyls (PCBs) in a

Jan 8, 2010 - Transformation of Chiral Polychlorinated Biphenyls (PCBs) in a Stream Food Web. Viet D. Dang ... Corresponding author phone: 864-656-100...
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Environ. Sci. Technol. 2010, 44, 2836–2841

Transformation of Chiral Polychlorinated Biphenyls (PCBs) in a Stream Food Web† V I E T D . D A N G , ‡ D A V I D M . W A L T E R S , §,| A N D C I N D Y M . L E E * ,‡ Department of Environmental Engineering and Earth Sciences, Clemson University, 342 Computer Court, Anderson, South Carolina 29625, and U.S. Environmental Protection Agency, National Exposure Research Laboratory, 26 West Martin Luther King Boulevard, Cincinnati, Ohio 45268

Received July 23, 2009. Revised manuscript received December 11, 2009. Accepted December 11, 2009.

The enantiomeric composition of chiral PCB congeners was determinedinTwelvemileCreek(Clemson,SC)toexaminepotential mechanisms of biotransformation in a stream food web. We measured enantiomeric fractions (EFs) of six PCB atropisomers (PCBs 84, 91, 95, 136, 149, and 174) in surface sediment, fine benthic organic matter (FBOM), coarse particulate organic matter (CPOM), periphyton, Asian clam, mayflies, yellowfin shiner, and semipermeable membrane devices (SPMDs) using gas chromatography (GC-ECD). Nonracemic EFs of PCBs 91, 95, 136, and 149 were measured in almost all samples. Enantiomeric compositions of PCBs 84 and 174 were infrequently detected with racemic EFs measured in samples except for a nonracemic EF of PCB 84 in clams. Nonracemic EFs of PCBs 91, 136, and 149 in SPMDs may be due to desorption of nonracemic residues from FBOM. EFs for some atropisomers were significantly different among FBOM, CPOM, and periphyton, suggesting that their microbial communities have different biotransformation processes. Nonracemic EFs in clams and fish suggest both in vivo biotransformation and uptake of nonracemic residues from their food sources. Longitudinal variability in EFs was generally low among congeners observed in matrices.

Introduction Polychlorinated biphenyls (PCBs) are a class of organochlorines (OCs) produced commercially by catalytic chlorination of biphenyls (1). Low aqueous solubility and high boiling point make PCBs truly global environmental pollutants. The total amount of commercial PCBs produced from 1920 to 1970 has been estimated at approximately 1.5 × 105 metric tons (2). Due to their persistent characteristics, PCBs tend to bioaccumulate in fatty tissues and biomagnify through the food web. Even though manufacture of PCBs ceased in 1977, they are still present at low concentrations in most environmental matrices (e.g., sediment, fish, and human blood). PCB contamination in freshwaters remains widespread, with 209,000 stream kilometers and nearly 2 million † Part of the special section “Sources, Exposures, and Toxicities of PCBs in Humans and the Environment”. * Corresponding author phone: 864-656-1006; fax: 864-656-0672; e-mail: [email protected]. ‡ Clemson University. § National Exposure Research Laboratory. | Present address: U.S. Geological Survey, Fort Collins Science Center, 2150 Centre Ave., Fort Collins, Colorado 80526.

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lake hectares under advisories for fish consumption in the U.S. alone (3). Chiral analysis has been introduced as a useful tool to investigate the biotransformation mechanisms of PCBs in the environment. Seventy-eight congeners are chiral, 19 of which are stable atropisomers (containing at least three or four chlorine atoms at ortho-positions) at room temperature (4). Enantiomers of an atropisomer have identical chemical and physical properties, but can exhibit different biological and toxicological properties. PCB atropisomers are released into the environment as racemates, but under microbial transformation or metabolic activity in higher organisms, one of the enantiomers will be selectively accumulated and the other will be transformed (5, 6). Most studies of chiral transformation have investigated food webs in marine or lentic systems (5, 7-9), and information regarding transformation processes in stream food webs is lacking. Streams are dynamic systems and it is unclear if microbial transformation or metazoan metabolism are important transformation processes or if transformation varies with longitudinal position along the river continuum (10). Identifying these processes is an important step in understanding the fate and transport of PCBs, not only within stream ecosystems but also within adjacent riparian zones and downstream water bodies that receive PCBs exported from streams (11-13). We conducted our research in the Twelvemile Creek section of the Sangamo-Weston/Twelvemile Creek/Lake Hartwell Superfund site. The site is listed on the National Priority List (NPL) for long-term remedial action as it appears to present a significant risk to public health, welfare, or the environment. To decrease PCBs concentration in the environment, natural attenuation was recommended as an efficient mechanism. Therefore, physiochemical and biochemical weathering could play a significant role in this system. Previous studies have investigated transformation of achiral PCBs congener patterns in Twelvemile Creek (13), and biotransformation of chiral PCBs in Lake Hartwell (9, 14-16), but chiral PCBs transformation has not been investigated in Twelvemile Creek. Our main objectives were to (1) identify transformation of those chiral congeners undergoing either microbial processing or species metabolism, and (2) consider longitudinal differences in chiral patterns. We hypothesized that both metabolism and microbial transformation contribute to the biotransformation of PCBs in Twelvemile Creek food web. Microbial transformation has been documented in numerous lake and marine systems (7, 9, 16). Lower trophic-level organisms (e.g., zooplankton, invertebrates) generally have little, if any, biotransformation capabilities toward xenobiotics, and enantiomer enrichment of chiral pollutants in these organisms typically mirrors the surrounding environment (17-19). However, Warner and Wong (8) indicated that a freshwater invertebrate can eliminate chiral organochlorine compounds enantioselectively. These limited observations suggest that lower organisms may have greater capability to biodegrade persistent contaminants than previously thought. More advanced organisms such as fish can metabolically transform chiral compounds, but results are inconsistent among species and between marine and freshwater systems (7, 20, 21). We also hypothesized that longitudinal differences in chiral signatures are minimal in a stream system. Transport of nonracemic atropisomers in lotic systems is possibly associated with physiochemical processes other than biochemical processes. According to Farley et al. (14), Twelvemile Creek is divided into an upper and lower reach (Supporting 10.1021/es902227a

 2010 American Chemical Society

Published on Web 01/08/2010

FIGURE 1. Simplified food web in Twelvemile Creek modified from Walters et al. (13) and Rybczynski et al. (24). CPOM coarse particulate organic matter; FBOM - fine benthic organic matter. Information Table S1). In the upper reach (0-30 km), which is our study section, the channel is relatively shallow (∼0.4 m) with an average width of 25 m, and water velocities are relatively high (∼0.6 m/s). In the lower reach (32-39 km), the creek deepens and widens because of the impoundment of Lake Hartwell. Because waters in the upper portion of Twelvemile Creek system are well oxygenated and the total organic carbon content of the sediments is low (0.1-3.6%), surface sediments are believed to remain aerobic. Given that opportunities for anaerobic transformation are low, that residence time for water within the upper reach are low (∼ 6 days), and that the fine, unconsolidated bed material is readily transported downstream during frequent high-flow events (e.g., 0.5 year recurrence interval floods), it is likely that the chiral signatures of atropisomers entering the food web is similar among sites.

Experimental Section Study Area. The Sangamo Weston/Twelvemile Creek/Lake Hartwell Superfund site is located in Pickens County, SC. The Sangamo-Weston plant manufactured capacitors from approximately 1955 to 1978 (22). Approximately 181.4 t of PCBs were released into Town Creek, a tributary of Twelvemile Creek and were subsequently transported downstream to Lake Hartwell, a reservoir on the Savannah River (22) (Figure S1). Food Web Characterization. Twelvemile Creek has a diverse community and complex food web containing >40 macroinvertebrates taxa and >25 fish species (13). We limited our investigation to three types of organic matter, two primary consumer macroinvertebrates, and one fish species (Figure 1). Coarse particulate organic matter (CPOM), fine benthic organic matter (FBOM), and periphyton are the main sources of organic matter to the stream food web. Asian clams (Corbicula fluminea) feed on fine particulate organic matter (i.e., FBOM) collected from sediments by pedal feeding or by filtering suspended fine particulate matter (i.e., seston) from the water column. Prior analysis demonstrated that δ13C and δ15N isotopes of seston and FBOM were very similar, suggesting that they constituted a single pool of carbon sources for the food web (23). “Mayflies” is limited to species in the genus Stenonema, which are grazers that consume periphyton. Yellowfin shiner (Notropis lutipinnis) is an omnivore, and a mixture of invertebrates, CPOM, FBOM, and periphyton comprised more than 95% of its diet in autumn when our samples were collected (24). FBOM also serves as a surrogate of the sediment compartment for the purpose of chiral analysis, because it is a concentrated sample of organic matter present in the stream bed. Sampling Methods. We sampled at four locations in the fall of 2005, except for FBOM samples, which were collected in 2003 and 2004. Collection sites were located from 3 to 25 km downstream of the Sangamo-Weston site (Figure S1). Three replicates of each matrix were collected at each sampling site. Detailed collection methods are provided

elsewhere (13, 23). Briefly, surface sediment (0-3 cm) was collected with a metal scoop from multiple depositional habitats within each site and composited (25). Additional sediment samples were retrieved for collection of FBOM. These sediments were thoroughly mixed, elutriated several times to remove the coarse fraction, and sieved to obtain organic matter 48 and 250 µm in size. CPOM (i.e., conditioned leaves) was collected by hand from the channel. Periphyton was collected from cobbles and woody debris. Cobbles and wood were gently rinsed by hand over a plastic pan, and the resulting slurry was collected. Mayflies were collected from a variety of habitats using nets or picking wood by hand. They were identified to genus in the field, and multiple individuals were composited into samples. Yellowfin shiners were collected by seining and backpack electrofishing, identified in the field, and composited into samples. Adult fish of a similar size ( 0.5) and 149 (EFs < 0.5), but different EFs for PCBs 84 and 95. Yellowfin shiner had racemic EF for PCB 174, while it had nonracemic EFs for PCBs 91, 136, and 149. EF for PCB 91 in yellowfin shiner was significantly different from its food sources FBOM, CPOM, and mayfly. Yellowfin shiner EF for PCB 149 was similar to mayfly, periphyton, and CPOM samples, but different from FBOM. No EFs for PCB 174 were measured in the food sources for yellowfin shiner. Variation in the longitudinal EFs was also examined in the matrices. EFs measured at all four sites were only observed in FBOM, yellowfin shiner, and SPMD. EFs in other samples were measured for at least two sites (Table S3). We found no significant difference in EFs among the four sites for these matrices (Tukey test, P < 0.05), except for EFs of PCB 91 in FBOM and yellowfin shiner, and for EF of PCB 136 in Asian clam (Figures S2 and S4).

Discussion Some congener concentrations were below the detection limit, so EFs were not quantifiable in all collected matrices. Surface sediment samples consisted primarily of sand and had low concentrations of all atropisomeric PCBs, resulting in no detection of any EFs in these samples. EF values were variable among congeners and matrices except for PCB 149 in which the (+)-enantiomer was more depleted than the (-)-enantiomer in all matrices. This suggests that PCB 149 was transferred through the food web without additional transformation. Most of the EFs measured deviated from 0.5 indicating that microbial processing controlled the transformation of PCBs in basal resources, while metabolism occurred in some Twelvemile Creek consumers. Microbial Transformation in Basal Resources. Enrichment or depletion of enantiomers found in sediment associated organic matter is evidence for microbial processes in the environment. Nonracemic residues of PCBs 136 and 149 in FBOM and CPOM, which are closely associated with sediment, suggest that microbial transformation is likely occurring in the basal resources of the stream food web. Although none of the atropisomeric PCBs were quantifiable in sediments, FBOM can serve as a surrogate because it is

FIGURE 2. Box plots of enantiomeric fractions (EFs) for four PCB atropisomers measured in Twelvemile Creek food web samples from four sites. EFs for atropisomers in sediment are not presented due to concentrations below detection limit. The data for PCBs 84 and 174 are shown only in Table S3. Values shown are mean EFs calculated among three replicate samples and sites whenever measured. EFs in deployed SPMD and Asian clam were average values measured after 10, 24, 40, and 60 days whenever possible. Horizontal line in each panel indicates racemic EFs (0.5). Separate letters indicate significantly different EFs. Asterisks indicate significantly nonracemic EFs. fbom, fine benthic organic matter; cpom, coarse particulate organic matter; spmd, semipermeable membrane device; peri, periphyton; clam, Asian clam; mayfly, Stenonema spp.; shiner, yellowfin shiner. a concentrated sample of organic matter present in the stream bed. Therefore, enantioselective processes in sediment can be inferred from enantioselective processes in FBOM. In previous work, PCB 91 was detected in sediment from Lake Hartwell, which is the receiving body for Twelvemile Creek (16). The EF of PCB 91 was about 0.36 (enantiomeric ratio (ER) of 0.56) at site G27, located 1.6 km from the mouth of Twelvemile Creek, to near racemic levels (EF ) 0.5 or ER ) 1.0) farther downgradient (site G46, 7.5 km) (16). The EF value of PCB 91 in Lake Hartwell sediment is reversed to that measured in Twelvemile Creek samples of FBOM. According to Wong et al. (15), the EFs of PCB 91 were racemic in sediment extracts in several streams sampled around the U.S. Both Wong et al. (15) and our present study used the same chiral column for analysis. Therefore, the inconsistent results among these studies likely reflect different enantioselective biodegradation among sediment locations. Differences in EF values among organic matter types (FBOM, CPOM, and periphyton) were also observed. These have different microbial communities in which FBOM is dominated by bacteria, CPOM is dominated by fungi, and periphyton is a complex mixture of autotrophs and heterotrophs (33). The EF of PCB 136 was >0.5 for FBOM and CPOM, while it was 0.5) were observed in phytoplankton collected from a Hudson River estuary food web (35). The only atropisomers detected in periphyton were PCBs 136 and 149, and both had EFs < 0.5. The EF for PCB 136 in the periphyton was significantly different from that in FBOM and CPOM suggesting that periphyton autotrophs were responsible for transformation. Likewise, EFs for SPMDs and periphyton were vastly different for PCB 136. Like SPMDs, periphyton sorbs PCBs from the water columns (14, 36, 37). Thus, large differences in EFs between these matrices provide strong evidence for in situ biotransformation within the periphyton microbial community. By contrast, EFs for PCB 149 are quite similar among matrices, indicating passive uptake of PCBs transformed elsewhere (e.g., sediment VOL. 44, NO. 8, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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microbial communities). Enantioselectivity of PCBs in fungi, which populates the CPOM, has not been considered in prior studies. EFs for PCBs 91 and 95 in CPOM are significantly different from those found in FBOM and SPMD, indicating that the fungi are transforming these congeners differently. Differences in EF signatures among these organic matter types imply that different stream microbial communities have different transformation processes. SPMDs are passive samplers used to collect dissolved contaminants in the water column. Racemic EF of PCBs 84 and 95 were only observed in SPMD suggesting atmospheric deposition or an additional unweathered source of PCBs (i.e., a potential groundwater to surface water transport path from the Sangamo-Weston plant) to the aquatic system. If we assumed that PCBs in the water column only came from atmospheric deposition, concentrations should be low and EF compositions of atropisomeric PCBs would be racemic because abiotic processes (e.g., volatilization, deposition) do not alter enantiomeric compositions. However, we found nonracemic EFs of PCBs 91, 136, and 149 in SPMDs. In addition, Asher et al. (35) measured, to some extent, nonracemic EFs of PCBs 95 and 149 in the dissolved phase. Therefore, desorption, resuspension, and excretion processes in sediment and biota could be attributed to nonracemic EFs in the dissolved phase. The trend of EFs in SPMD is more similar to FBOM than other matrices. This suggests the nonracemic EFs observed in SPMD result from uptake of nonracemic residues from FBOM, either through sediment suspension or desorption of PCBs transformed in sediments. Metabolic Transformation in Consumers. Changes in EFs between consumers and their diet indicate in vivo metabolism, and we found some evidence of the process in Twelvemile Creek. Clams or bivalves are filter-feeders consuming particulate-bound PCBs in the water column or in sediments. EFs of PCBs 136 and 149 were similar between clams and FBOM, while those of PCBs 84 and 95 were significantly different. This finding points to metabolism by clams and is consistent with prior findings for other stream bivalves (15). However, data are limited for this important group of aquatic primary consumers. Aquatic insects are abundant, ubiquitous, and productive organisms providing a vital link between basal organic matter sources and higher trophic levels in aquatic food webs. In spite of their ecological importance, their role in transforming PCBs and other chiral contaminants has not been assessed. Our study produced little evidence for enantioselective bioprocessing in mayfly. The Stenonema mayflies we evaluated are grazers which feed primarily on periphyton. EF values for PCBs 91 and 95 were racemic and nonracemic in mayfly, respectively, while neither PCBs 91 nor 95 was detected in periphyton. We are not able to assess transformation of PCBs 91 and 95 in mayfly, because they were not detected in its diet, periphyton. In addition, there is little evidence from the literature to support metabolism of PCBs in insects. PCB 149 was the only chiral congener measured in both mayfly and periphyton with a similar EF value for both matrices. EFs for PCB 149 varied little among food web compartments in Twelvemile Creek, suggesting uptake of nonracemic residues from prey to consumers. However, metabolism cannot be ruled out. The enantiomeric compositions of PCBs in yellowfin shiner are likely due to a combination of uptake of nonracemic residues from the diet and in vivo metabolism. Yellowfin shiners consume FBOM, CPOM, periphyton, and mayfly (24) and may uptake nonracemic residue from any of these food resources. However, yellowfin shiner had a significantly lower EF for PCB 91 than FBOM, CPOM, and mayfly, suggesting that they are stereoselectively biotransforming PCB 91. The EF value for PCB 149 in yellowfin shiner was statistically different from that in FBOM, but not from 2840

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its other food sources. The EF signature of PCB 136 in yellowfin shiner was significantly different from that in periphyton, but not from its other dietary items. This suggests that yellowfin shiner has limited capability for metabolizing the more chlorinated PCBs 136 and 149, but this is difficult to directly assess given the diversity of items in their diet. Previous studies (21, 38, 39) indicated that fish can selectively biotransform PCB 136. Longitudinal EFs within Matrices. Changes in EFs with distance provide insight into the mechanisms of microbial transformation and physiochemical weathering. The longitudinal variability was generally low among congeners and among-site differences were only observed for PCB 91in FBOM and yellowfin shiner, and PCB 136 in Asian clam (Figures S2-S5). In Lake Hartwell system, Wong et al. (9) observed some changes in EFs between two locations (i.e., sites G27 and G46) in surface sediments. Physical processes in the lake including turbulent mixing and burial may contribute to spatial variation in EFs in surface sediments. In addition, EFs differ with depth in Lake Hartwell cores sampled at several locations, suggesting a spatial distribution of different microbial communities. Nonetheless, little data are available to examine longitudinal EFs in either lake or stream systems. We hypothesized two possibilities that could result in, to some extent, similar EFs with distance in the stream system. First, depositional habitats in Twelvemile Creek are limited indicating a homogeneous composition of sediment, which is dominated by sand (23). Given the similar depositional habitats, mechanism of PCBs microbial transformation could be similar for a given organic matter type. Second, the movement of PCBs is likely dominated by sediment transport during high flow events, little or no net sedimentation is believed to occur in the upper reach of Twelvemile Creek. Biochemical weathering through reductive dechlorination is, therefore, not expected to be significant in surface sediments, and is consistent with our findings that EFs within food web compartments showed little spatial variability. However, high concentrations of PCBs were still measured in the matrices suggesting that a potential source of the contaminants is entering the system. Potential PCBs might be coming from riparian zone (e.g., disposal landfills, contaminated plants, and so on), and then entering into the stream during high flow events. Another possibility is the contribution of groundwater contamination from an abandoned wastewater facility located in Town Creek. This observation was also discussed by Walters et al. (13). This is the first study to comprehensively examine biotransformation of PCBs in a stream food web system. Our observations of nonracemic EFs suggest some degree of PCB biotransformation in aquatic biota in Twelvemile Creek. The EF measurements revealed that metabolism is occurring simultaneously with enantioselective microbial processing in different organic matter pools within Twelvemile Creek. Some previous research concluded that the most likely mechanism governing a change in EFs between predator and prey is enantioselective biotransformation, if the diet of the predator is well-characterized (7, 38, 40). To our knowledge, we observed the first occurrence of microbial processing among different microbial communities associated with different organic matter types. We also provided additional evidence of the ability of clams and fish to metabolize PCBs, at least to some degree. Further research is needed to evaluate the capability of mayflies and other aquatic insects in metabolizing chiral pollutants such as PCBs, because these insects play a vital role in transferring energy and contaminants through freshwater aquatic and riparian food webs.

Acknowledgments We appreciate the comments from the anonymous reviewers. Support for this work was provided by the National Science Foundation (CBET-0828699) and the U.S. Environmental Protection Agency (contract 218-2095072). This research was subjected to U.S. EPA review and approved for publication.

Supporting Information Available Methods for determining lack of interferences for chiral analysis, mapofthestudyarea,figuresofvariationsofEFsforfourcongeners among matrices and sampling sites, and tables of concentrations of total PCB and chiral congeners. This material is available free of charge via the Internet at http://pubs.acs.org.

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