Evidence for Anaerobic Dechlorination of ... - ACS Publications

Nov 16, 2015 - Ministry of the Environment, Toronto, Ontario M9P 3 V6, Canada ... The environmental occurrence of dechlorination moieties from the hig...
0 downloads 0 Views 886KB Size
Download PDF
Article pubs.acs.org/est

Evidence for Anaerobic Dechlorination of Dechlorane Plus in Sewage Sludge Ed Sverko,*,†,‡ Brian McCarry,†,# Robert McCrindle,∇ Allison Brazeau,∇ Miren Pena-Abaurrea,⊥ Eric Reiner,⊥ Shirley Anne Smyth,‡ Biban Gill,§ and Gregg T. Tomy∥ †

Department of Chemistry and Chemical Biology, McMaster University, Hamilton, Ontario L8S 4M1, Canada Water Science and Technology Directorate, Environment Canada, Burlington, Ontario L7R 4A6, Canada § Department of Biological Sciences, University of Toronto Scarborough Campus, Toronto, Ontario, M1C 1A4, Canada ∥ Department of Chemistry, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada ⊥ Ministry of the Environment, Toronto, Ontario M9P 3 V6, Canada ∇ Wellington Laboratories, Guelph, Ontario N1G 3M5, Canada ‡

S Supporting Information *

ABSTRACT: The environmental occurrence of dechlorination moieties from the high production volume flame retardant, Dechlorane Plus (DP), has largely been documented; however, the sources have yet to be well understood. In addition, few laboratory-based studies exist which identify the cause for the occurrence of these chemicals in the environment or humans. Anaerobic dechlorination of the two DP isomers was investigated using a laboratory-simulated wastewater treatment plant (WWTP) environment where anaerobic digestion is used as part of the treatment regime. Known amounts of each isomer were added separately to sewage sludge which provided the electron-donating substrate and at prescribed time points in the incubation, a portion of the media was removed and analyzed for DP and any dechlorination metabolites. After 7 days, monohydrodechlorinated products were observed for both the syn- and anti-DP which were continued throughout the duration of our study (49 days) in an increasing manner giving a calculated formation rate of 0.48 ± 0.09 and 0.79 ± 0.12 pmols/day for syn- and anti-DP, respectively. Furthermore, we observed a second monohydrodechlorinated product only in the anti-DP isomer incubation medium. This strongly suggests that anti-DP is more susceptible to anaerobic degradation than the syn isomer. We also provide compelling evidence to the location of chlorine loss in the dechlorination DP analogues. Finally, the dechlorination DP moieties formed in our study matched the retention times and identification of those observed in surficial sediment located downstream of the WWTP.

■

(PBDE).5 Deliberations are still ongoing for deca-BDE largely because of the known PB&T nature of its debrominated products. The purported benefits of FRs have given rise to the widespread application of these chemicals to a broad range of consumer products in the last several decades. A recent example of this is the chlorinated flame retardant, Dechlorane Plus (DP). First reported by Hoh et al. in 2006, DP has since been shown to be a worldwide contaminant.6−8 The estimated annual production for DP at its North American plant

INTRODUCTION A chemical once released into the environment is susceptible to a variety of environmental transformational pathways that can affect its persistence (P), bioaccumulation (B), and toxicity (T). Postrelease fate of these chemicals, such as photolytic and microbial degradation, can alter the original chemical to forms that have different physical-chemical properties which often result in these transformation products residing in unintended and unexpected areas. Historical examples of these anthropogenic chemicals detected (both parent and metabolites) in the environment are well documented.1−4 The Stockholm Convention, which came into effect in 2004, is aimed at regulating the release of PB&T chemicals into the environment and also includes any disconcerting transformational products. At their annual meeting in 2009, delegates agreed to restrict two formulations of the flame retardant (FR) polybrominated diphenyl ether © XXXX American Chemical Society

Special Issue: Ron Hites Tribute Received: July 22, 2015 Revised: November 9, 2015 Accepted: November 16, 2015

A

DOI: 10.1021/acs.est.5b03550 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology

added to ensure no 13C DP existed in the natural sludge used in this study. Using the protocol by Young and Tabak, an autoclaved control was not included in the study and, therefore, abiotic dechlorination of DP cannot be ruled out no matter how unlikely. We believe that the overriding anaerobic condition would much more readily provide dehalogenation conditions rather than any abiotic reaction. To ensure anaerobic conditions were maintained during the study, air within the headspace of the bottle was expunged using a venting system which allowed purified N2 (g) to fill the headspace as fully described elsewhere.18 Each of the jars was placed simultaneously on an incubated shaker-table (Fisher Scientific, Ottawa, ON) at 35 °C (± 1 °C). These were kept at the same condition until such time removal was required. One bottle for each 13C DP isomer was removed from the shakertable every 7 days and frozen (−20 °C) until analysis; totaling a digestion period of 49 days. Extraction and Analysis. Mirex (Sigma-Aldrich, Oakville, ON) in methanol was added to each of the thawed sewage digestion mixtures as an extraction performance standard. Dichloromethane (50 mL) was then added and mixed with the digestion mixture in a shaker table for 3 min, passed through dried sodium sulfate before being collected in a 250 roundbottom flask; this process was repeated twice. Five mL of isooctane were added to the round-bottom flask prior to evaporation and reduced to approximately 3 mL. The sample was quantitatively transferred to a centrifuge tube and evaporated to 1 mL. The sample was then added to a 10 g fully activated Si gel column which was capped with 2 cm of sodium sulfate. Sixty mL of dichloromethane/hexane (1:1 v/v) were eluted through and collected in a 100 mL round-bottom flask. Following a 5 mL addition of isooctane, the sample was evaporated to approximately 3 mL and quantitatively transferred to a centrifuge tube where it was concentrated to 1 mL. One-microlitre injections were made into an Agilent 5980 gas chromatograph (GC) coupled to an Agilent 5973 mass spectrometer (MS) operated in electron capture chemical ionization mode using methane as a moderating gas. The GC was fitted with a 30 m DB-5 capillary column (0.25 μm film thickness × 0.25 mm i.d.; J&W Scientific, Folsom, CA) using helium as the carrier gas. The initial oven temperature was set at 80 °C with a 2 min hold time, ramped at 10 °C/min to 285 °C and held for 15 min. Source and quadruple temperatures were set to 150 and 106 °C, respectively. 13C DP was detected by monitoring for m/z 662.8, 664.8, and 666.8, whereas the hydrodechlorinated moieties, 13C Cl11-DP, were determined using m/z ions 628.7/630.7/632.7. All results are reported on a dry weight basis. Sediment Collection and Analysis. Detailed information has been previously published by Pena-Abaurrea et al.20 Briefly, the top 3−5 cm of river or stream sediment was collected in the middle of the waterway throughout southern Ontario, Canada. Samples were filtered with a 1.25 cm metal sieve then stored at −20 °C until analysis. Prior to extraction, samples were airdried for 24 h and further filtered through a 2 mm metal sieve. Once fortified with isotopically labeled PCB and PBDE surrogates, the sediment underwent Soxhlet extraction for 16 h using 400 mL toluene. Following concentration to a reduced volume, extracts were purified using elemental copper then eluted through a mulit-layer silica column (acidic, neutral and basic) and a subsequent clean up using florisil; extracts were brought down to a final volume of 1 mL. Analysis for the sediment samples were conducted in conjunction with the

(OxyChem, NY) is as high as 10 million pounds. Surprisingly, Wang et al. reported in 2010 on a second DP manufacturing plant located in China, confounding accurate global production volumes.9 That the European Commission identified DP as a possible replacement for deca-BDE suggests future production volumes will likely increase.10 The United States Environmental Protection Agency has designated this flame retardant as a High Production Volume chemical, while Canada has included DP on its Canadian Domestic Substances list. DP is primarily used in hard plastic connectors in televisions and computer monitors, wire coatings and furniture.8 Recent research has shown that DP caused a generalized stress response as well as affecting the metabolic process in juvenile Chinese sturgeon, whereas Wu et al. reported on DP’s toxicological effects at the transcriptomic and metabonomic levels in mice.11,12 DP and its dechlorinated analogues have also been found in human serum including the maternal transfer of these compounds to the fetus.13−15 In 2007, we first published data on several hydrodechlorinated-DP products in suspended sediment of the Niagara River, at a location downstream of OxyChem.16 Subsequent search of the literature identified an industrial wastewater treatment plant (WWTP) that receives wastewater effluent from OxyChem.17 This wastewater stream entering the WWTP is exposed to anaerobic conditions before being released into the receiving waters of the Niagara River.8 Based on these observations, we hypothesized that anaerobic degradation of DP leads to formation of dechlorination products. To test this hypothesis, we individually incubated both isomers of DP in a controlled anaerobic environment using sewage sludge as the electron-donating substrate. The results of our study provide compelling evidence of in situ formation for several monohydrodechlorinated products that were formed and confirmed using authentic synthesized standards by mass spectrometry. We also show that these products exist in the sediment collected downstream of the WWTP.To our knowledge this is the first paper identifying DP dechlorination products formed in an anaerobic laboratorybased study.

■

MATERIALS AND METHODS Digestion. Details of preparation and procedures for the methanogenic anaerobic digestion can be found elsewhere.18 Briefly, both 13C-labeled syn- and anti-DP (Cambridge Isotope Laboratories Inc. Tewksbury, MA) were added separately (2.0 nmoles) to two 3.0 g collections of dried sludge. Using the addition of acetone as the intermediary, the mixture was mixed on a shaker table for 0.5 h to help distribute the isotopically labeled DP isomers evenly within the sludge particulate; the two mixtures were air-dried for 12 h. DP, possessing a log KOA of 14, would overwhelmingly not evaporate but rather be adsorbed onto the sludge particulate.19 Dosing concentrations were then determined by weight of particulate giving an exact measured weight of approximately 0.1 g. This 13C DP-laden amount was then added to 65 mL of sewage sludge and mixed thoroughly in a 100 mL incubator bottle (Agilent Technologies, Mississauga, ON). Fifteen milliliters of anaerobic sludge (seed) was added to each of the incubator bottles as a cosubstrate to begin the anaerobic digestion. Seven bottles for each 13C DP isomer were prepared accordingly along with one replicate, collected at day 49, and 3 controls, collected on days 0, 21, and 49. The controls were prepared similarly to the other digestion samples but without the addition of DP. These controls were B

DOI: 10.1021/acs.est.5b03550 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology anaerobic digestion samples. DP was detected by monitoring for m/z 649.8, 651.8, and 653.8 while the hydrodechlorinated moieties, Cl11-DP(-Cl+H) and Cl10-DP(−2Cl+2H) were determined using m/z ions 615.7/617.7/619.7 and 581.8/ 583.8/585.8, respectively. Quality Assurance/Quality Control. For the anaerobic digestion analysis, neither 13C labeled syn- nor anti-DP were detected in the control samples. Two laboratory extraction blanks using Ottawa sand (Fisher Scientific) carried out during the extraction procedure did not detect any 13C DP isomers. Percent recoveries for mirex ranged from 81−103% while for the two laboratory blank spikes (Ottawa sand), recoveries for both 13C labeled syn- and anti-DP were 78−109%. The day 49 replicates gave a percent difference of 23 and 35 for the syn and anti isomers, respectively. For the sediment analysis, one method blank, method blank spike and a certified reference material (NIST 1944) were included with every 20 samples. No DP isomers were detected in the laboratory blanks or their dechlorination products. Spike recovery ranges for the labeled PCBs and PBDEs were 43− 132% and 65−86%, respectively. Quantitation is based on an external standard method calibrated against a multipoint curve giving a dynamic range of 10−2000 pg on column (r2 > 0.990). Monohydrodechlorinated DP compounds were calculated against analytical grade monohydrodechlorinated anti-DP (Wellington Laboratories, Guelph, ON); it was assumed that the syn dechlorination product was equi-responsive and calculated against the dechlorinated anti-DP analytical standard. Dechloro-DP Structure Elucidation. The three dechlorination DP products identified in the anaerobic digestion study were synthesized by proprietary methods at Wellington Laboratories and their structures defined, unambiguously, by single crystal X-ray diffraction.

Figure 1. Amount of 13C syn-DP-Cl (exo) formed during the 49 day digestion study period.

pmols, respectively, and at all sampling points thereafter (Figure 2).

■

RESULTS AND DISCUSSION The target compounds measured in our fortified incubation media were all undetectable in our control medium. Not surprisingly, we were able to measure 13C syn-DP at every sampling point in our incubation medium (Figure S1). After 14 days, molar amounts of 13C syn-DP remained relatively unchanged with an average measured amount of 1.47 ± 0.08 nmol (arithmetic mean ±1 × standard error). A monohydrodechlorinated 13C syn-DP metabolite, 13C syn-DP-Cl, was measurable after 7 days of incubation. Molar amounts of the dechlorinated metabolite at day seven was 3 pmols and increased linearly (r2 = 0.860, p < 0.05) to a maximum molar amount of 25 pmols on the final sampling point (Figure 1). The rate at which this compound was formed was calculated to be 0.48 ± 0.09 pmols/day. The overall conversion rate of the parent compound to this metabolite calculated from the slope of a plot of amount of metabolite over the amount of parent versus time yielded a valued of 0.03 ± 0.01% per day (p < 0.05). On days seven and 14, molar amounts of 13C anti-DP were 0.5 and 0.7 pmols, respectively. We then observed an increase to 1.7 pmols at day 21 followed by a leveling off until the end of our experiment giving a mean amount of 1.31 ± 0.19 pmols (arithmetic mean ±1 × standard error). Two monohydrodechlorinated metabolites were detected that were confirmed using authentic external standards. Both metabolites, herein identified as 13C anti-DP-1Cl (exo) and 13C anti-DP-1Cl(endo), were detectable first at day seven at a molar amount of 4 pmols and 2

Figure 2. Amount of 13C anti-DP-Cl (exo) and 13C anti-DP-Cl(endo) formed during the 49 day digestion study period.

The formation of 13C anti-DP-1Cl (exo) was found to increase in a linear manner (r2 = 0.901, p < 0.05) with a calculated rate of formation of 0.79 ± 0.12 pmols/day. The second metabolite, 13C anti-DP-1Cl(endo), also increased linearly (r2 = 0.85, p < 0.05) to a maximum of 23 pmols at day 49 (Figure 2). The calculated rate of formation for this metabolite, 0.4 ± 0.1 pmols/day, was two times smaller than that of 13C anti-DP-1Cl. The overall conversion rate of the parent compound to the metabolite was calculated to be 0.03 ± 0.04% per day (p < 0.05). While we could not identify the cause for the lower initial amounts of syn- and anti-DP in the first one and two time points, respectively, in the digestion study, we believe this did not affect the formation kinetics because (i) we intentionally spiked at a high concentration so as to provide an overabundance of material for the microbes to metabolize, (ii) the high degree of linearity and significance in all three dechlorination metabolites is evidence that the transformation rates were not affected, and (iii) the resultant metabolite amounts were 3 orders of magnitude lesser than the DP isomers. We also observed a lower than expected value on day 42 for all formation products. After reinjection of same extracts, the results were unchanged. As well, upon review of laboratory and instrumental notes, no anomalies were identified. We can C

DOI: 10.1021/acs.est.5b03550 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology

We have identified the three dechlorination metabolites and their geminal Cl positions as the following: 13C syn-DP-Cl (exo), 13C anti-DP-1Cl (exo), 13C anti-DP-1Cl (endo) (Figure 4). Based on the text above, the implied degree of steric

Figure 4. Structure identification of the three dechlorination metabolites created from the anaerobic digestion of DP: A. syn-DPCl (exo), B. anti-DP-Cl (endo), C. anti-DP-Cl (exo). Nonessential hydrogens are removed for clarity.

hindrance would be 13C anti-DP-1Cl(endo) > 13C syn-DP-Cl > 13 C anti-DP-1Cl (exo). This is corroborated nicely with our current study as the greatest (quickest) rate of formation is 13C anti-DP-1Cl (exo) and the least (slowest) rate of formation is that of 13C anti-DP-1Cl(endo). In 2007 we first reported on mono- and dihydrodechlorinated DP compounds in Niagara River suspended sediments collected in 2002.16 This sampling station (NOTL) was located downstream of OxyChem and an industrial WWTP (Figure S2). Further research revealed that OxyChem fed their process wastewater to the WWTP created in 1985 to reduce the toxicity of the original chemicals contained in the wastewater before release into the Niagara River.22 This WWTP was known to expose the waste stream to an anaerobic environment as part of its treatment regime. Anaerobic media are well-known to produce a reductive environment for compounds which results in the production of dehalogenated, and ostensibly less toxic, products.18,21,23,24 Samples taken concurrently at an upstream station, Fort Erie (Figure S2) did not contain the dechlorinated DP analogues in detectable amounts indicating that these compounds were introduced to the waterway at a point, or points, in between the sampling stations. However, these dechlorinated DP analogues were detected inconsistently at the NOTL sampling station over the sampled period (1 year) suggesting the source(s) for these compounds was of a variable nature. One conceivable possibility was that OxyChem manufactured DP in a “batch” process and not continuously−this then would result in the related process wastewater to also be released to the WWTP in a periodic manner. While our anaerobic digestion study did not produce as numerous amounts of dechlorination products found in the

Figure 3. A. TIC Chromatogram of day-49 of the 13C anti-DP digestion study. The first red arrow corresponds to 13C anti-DP-1Cl (exo) and the second 13C anti-DP-1Cl (endo); B. TIC Chromatogram of day-49 of the 13C syn-DP digestion study. The blue arrow corresponds to 13C syn-DP-1Cl (exo); C. The matching corresponding compounds in a suspended sediment.

therefore not conclude why this dip occurred, however, this did not affect the overall trend given by the other six experimentally derived points. The stereo conformation of the DP isomers are colloquially described as “boat” for syn-DP and “chair” for anti-DP. While these isomers have the same molecular formula, their structures differ significantly as the boat/chair conformations reflect the shape of the cyclooctane center backbone. The “chair” conformation of anti-DP results in the four geminal chlorines point in the opposite direction, whereas for syn-DP, these same geminal chlorines pointing in the same direction. The stereochemistry for anti-DP, therefore, is less sterically hindered. It has been shown that compounds with geminal chlorine atoms, such as toxaphene, suffer anaerobic hydrodechlorination that is regiospecific in nature.21 In the present situation one might anticipate that replacement of an exo-Cl by hydrogen would be preferred since an atom with this orientation is less hindered sterically than its endo counterpart. D

DOI: 10.1021/acs.est.5b03550 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Environmental Science & Technology

■

Niagara River suspended sediment, nor any dihydrodechlorination products, we have shown the anaerobic formation of these compound types as a proof of concept. Other anaerobic microbial medialike in the WWTP receiving OxyChem wastewaterlikely contain a different variety of microbes which may be more virulent in dehalogenating organic compounds. As pointed out by one of the astute reviewers of this manuscript, other sources such as combined sewer outflows (CSO) release untreated sewage into the Niagara River. Others have shown that PCBs are readily dechlorinated by bacteria existing in combined sewers;25,26 by extension, this too can occur with the DP isomers creating dechlorinated compounds perhaps even with the removal of two chlorines. This may provide another reason why the existence of the dechlorinated compounds are so variable; raw sewage may only be released during storm events. As one considers this, it is important to note that our paper was not meant to establish the WWTP as the only source of these compounds, but at least the strong likelihood as being one of them. The sediment samples analyzed in this paper serves as a firstscreen surveillance only and to further prove that these dechlorination compounds exist today in different river and stream systems. Analyzing a greater number of sediment samples is beyond the scope of this research. The concentrations of syn-DP in the sediment were 0.57− 2.04 ng/g while for anti-DP the range was 0.84−6.49 ng/g. All three dechlorination DP analogues in this study were detected in all sediment samples. Concentration ranges for syn-DP-1Cl (exo), anti-DP-1Cl (exo), anti-DP-1Cl (endo) were 0.046− 0.833 ng/g, 0.70−2.00 ng/g and 0.155−1.08 ng/g, respectively. Note that the dechlorination compound identified by this anaerobic digestion study, anti-DP-1Cl (endo), as the one possessing the greatest steric hindrance and, therefore, less likely to form is not the least in concentration in these sediment samples. This speaks to the difficulty in applying any source apportionment approaches for these dechlorination DP analogues. Different environments possess different biological systems and therefore differing fate chemistries. Once released into the environment, the original compound profile can change over time confounding any forensic analysis. Implications. While anaerobic wastewater treatment systems may dehalogenate certain toxic substances to their lesser harmful products,25,26 other substances undergoing the same process may not transform to the same innocuous result. Given the recent research showing DP’s toxicity, the question now remains as to whether the properties of these dechlorination analogues possess similar or differing toxicological effects. Now that these three dechlorination DP analogues have been isolated by Wellington Laboratories, it would be beneficial to confirm the identity of these compounds in biota and whether, then, further toxicological studies would be warranted using these purified solutions.

■

Article

AUTHOR INFORMATION

Corresponding Author

*Phone: 905-336-4423; fax: 905-336-6404; e-mail: ed.sverko@ canada.ca. Notes

The authors declare no competing financial interest. # B.M. is deceased.

■

REFERENCES

(1) Venkatesan, A. K.; Halden, R. U. Wastewater Treatment Plants as Chemical Observatories to Forecast Ecological and Human Health Risks of Manmade Chemicals. Sci. Rep. 2014, 4.10.1038/srep03731 (2) Gutleb, A. C.; Cenijn, P.; Velzen, M. v.; Lie, E.; Ropstad, E.; Skaare, J. U.; Malmberg, T.; Bergman, A.; Gabrielsen, G. W.; Legler, J. In Vitro Assay Shows That PCB Metabolites Completely Saturate Thyroid Hormone Transport Capacity in Blood of Wild Polar Bears (Ursus maritimus). Environ. Sci. Technol. 2010, 44 (8), 3149−3154. (3) Verreault, J.; Gabrielsen, G. W.; Chu, S.; Muir, D. C. G.; Andersen, M.; Hamaed, A.; Letcher, R. J. Flame Retardants and Methoxylated and Hydroxylated Polybrominated Diphenyl Ethers in Two Norwegian Arctic Top Predators:Glaucous Gulls and Polar Bears. Environ. Sci. Technol. 2005, 39 (16), 6021−6028. (4) Letcher, R. J.; Norstrom, R. J.; Muir, D. C. G. Biotransformation versus Bioaccumulation:Sources of Methyl Sulfone PCB and 4,4’-DDE Metabolites in the Polar Bear Food Chain. Environ. Sci. Technol. 1998, 32 (11), 1656−1661. (5) Update to Canada’s National Implementation Plan under the Stockholm Convention on Persistent Organic Pollutants. 2015. https://ec.gc.ca/lcpe-cepa/default.asp?lang=En&n=FDB6031D1&offset=2&toc=show. (6) Moeller, A.; Xie, Z.; Sturm, R.; Ebinghaus, R. Large-Scale Distribution of Dechlorane Plus in Air and Seawater from the Arctic to Antarctica. Environ. Sci. Technol. 2010, 44 (23), 8977−8982. (7) Moeller, A.; Xie, Z.; Cai, M.; Sturm, R.; Ebinghaus, R. Brominated Flame Retardants and Dechlorane Plus in the Marine Atmosphere from Southeast Asia toward Antarctica. Environ. Sci. Technol. 2012, 46 (6), 3141−3148. (8) Sverko, E.; Tomy, G. T.; Reiner, E. J.; Li, Y. F.; McCarry, B. E.; Arnot, J. A.; Law, R. J.; Hites, R. A. Dechlorane Plus and Related Compounds in the Environment: A Review. Environ. Sci. Technol. 2011, 45 (12), 5088−5098. (9) Wang, D. G.; Yang, M.; Qi, H.; Sverko, E.; Ma, W. L.; Li, Y. F.; Alaee, M.; Reiner, E. J.; Shen, L. An Asia-specific source of dechlorane plus: Concentration, isomer profiles. Environ. Sci. Technol. 2010, 44 (17), 6608−6613. (10) Sverko, E.; Tomy, G. T.; Reiner, E. J.; Li, Y. F.; McCarry, B. E.; Arnot, J. A.; Law, R. J.; Hites, R. A. Dechlorane Plus and Related Compounds in the Environment: A Review. Environ. Sci. Technol. 2011, 45 (12), 5088−5098. (11) Liang, X.; Li, W.; Martyniuk, C. J.; Zha, J.; Wang, Z.; Cheng, G.; Giesy, J. P. Effects of dechlorane plus on the hepatic proteome of juvenile Chinese sturgeon (Acipenser sinensis). Aquat. Toxicol. 2014, 148, 83−91. (12) Wu, B.; Liu, S.; Guo, X.; Zhang, Y.; Zhang, X.; Li, M.; Cheng, S. Responses of mouse liver to dechlorane plus exposure by integrative transcriptomic and metabonomic studies. Environ. Sci. Technol. 2012, 46 (19), 10758−10764. (13) Ben, Y. J.; Li, X. H.; Yang, Y. L.; Li, L.; Di, J. P.; Wang, W. Y.; Zhou, R. F.; Xiao, K.; Zheng, M. Y.; Tian, Y. Dechlorane Plus and its dechlorinated analogs from an e-waste recycling center in maternal serum and breast milk of women in Wenling, China. Environ. Pollut. 2013, 173, 176−181. (14) Ben, Y. J.; Li, X. H.; Yang, Y. L.; Li, L.; Zheng, M. Y.; Wang, W. Y.; Xu, X. B. Placental Transfer of Dechlorane Plus in Mother-Infant Pairs in an E-Waste Recycling Area (Wenling, China). Environ. Sci. Technol. 2014, 48 (9), 5187−5193. (15) Siddique, S.; Xian, Q.; Abdelouahab, N.; Takser, L.; Phillips, S. P.; Feng, Y. l.; Wang, B.; Zhu, J. Levels of dechlorane plus and

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.5b03550. Figures S1 and S2; Table S1 (PDF) E

DOI: 10.1021/acs.est.5b03550 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

Article

Environmental Science & Technology polybrominated diphenylethers in human milk in two Canadian cities. Environ. Int. 2012, 39 (1), 50−55. (16) Sverko, E.; Tomy, G. T.; Marvin, C. H.; Zaruk, D.; Reiner, E.; Helm, P. A.; Hill, B.; McCarry, B. E. Dechlorane Plus Levels in Sediment of the Lower Great Lakes. Environ. Sci. Technol. 2007, 42 (2), 361−366. (17) Occidental Chemical Corporation- Buffalo Avenue. 2015. http://www.epa.gov/region2/waste/fsoccide.htm. (18) Young, J. C.; Tabak, H. H. Multilevel Protocol for Assessing the Fate and Effect of Toxic Organic Chemicals in Anaerobic Treatment Processes. Water Environ. Res. 1993, 65 (1), 34−45. (19) Zhu, J.; Feng, Y. l.; Shoeib, M. Detection of Dechlorane Plus in Residential Indoor Dust in the City of Ottawa, Canada. Environ. Sci. Technol. 2007, 41 (22), 7694−7698. (20) Pena-Abaurrea, M.; Jobst, K. J.; Ruffolo, R.; Shen, L.; McCrindle, R.; Helm, P. A.; Reiner, E. J. Identification of potential novel bioaccumulative and persistent chemicals in sediments from Ontario (Canada) using scripting approaches with GC x GC-ToF MS analysis. Environ. Sci. Technol. 2014, 48 (16), 9591−9599. (21) Ruppe, S.; Neumann, A.; Vetter, W. Anaerobic transformation of compounds of technical toxaphene. I. Regiospecific reaction of chlorobornanes with geminal chlorine atoms. Environ. Toxicol. Chem. 2003, 22 (11), 2614−2621. (22) The Niagara Falls Water Board Wastewater Facility information. 2015. http://www.nfwb.org/wastewater/html/approval.htm. (23) Li, Z.; Suzuki, D.; Zhang, C.; Yoshida, N.; Yang, S.; Katayama, A. Involvement of Dehalobacter strains in the anaerobic dechlorination of 2,4,6-trichlorophenol. J. Biosci. Bioeng. 2013, 116 (5), 602−609. (24) Seeger, M.; Hernandez, M.; Mandez, V.; Ponce, B.; Cardova, M.; Gonzalez, M. Bacterial degradation and bioremediation of chlorinated herbicides and biphenyls. Journal of soil science and plant nutrition 2010, 10 (3), 320−332. (25) Rodenburg, L. A.; Du, S.; Lui, H.; Guo, J.; Oseagulu, N.; Fennell, D. E. Evidence for dechlorination of polychlorinated biphenyls and polychlorinated dibenzo-p-dioxins and -furans in wastewater collection systems in the New York metropolitan area. Environ. Sci. Technol. 2012, 46 (12), 6612−6620. (26) Rodenburg, L. A.; Du, S.; Fennell, D. E.; Cavallo, G. J. Evidence for widespread dechlorination of polychlorinated biphenyls in groundwater, landfills, and wastewater collection systems. Environ. Sci. Technol. 2010, 44 (19), 7534−7540.

F

DOI: 10.1021/acs.est.5b03550 Environ. Sci. Technol. XXXX, XXX, XXX−XXX