Intrinsic Debromination Potential of Polybrominated Diphenyl Ethers in

Mar 28, 2014 - The half-lives of BDE-153 in eight different sediments varied from 7.6 to 165 days, with higher debromination in mangrove than marine a...
0 downloads 12 Views 1MB Size
Article pubs.acs.org/est

Intrinsic Debromination Potential of Polybrominated Diphenyl Ethers in Different Sediment Slurries Haowen Zhu,† Ying Wang,† Xiaowei Wang,‡ Tiangang Luan,‡ and Nora F. Y. Tam*,†,§ †

Department of Biology and Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong Special Administrative Region, People’s Republic of China ‡ MOE Key Laboratory of Aquatic Product Safety, School of Marine Sciences, Sun Yat-Shen University, Guangzhou 510275, People’s Republic of China § State Key Laboratory in Marine Pollution, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong Special Administrative Region, People’s Republic of China S Supporting Information *

ABSTRACT: The fate of BDE-153 (BDE = brominated diphenyl ethers) in different mangrove, fresh water pond, and marine subsurface sediments collected from Hong Kong SAR was investigated. Under anaerobic conditions, all sediments showed good intrinsic abilities to reductively debrominate BDE-153, producing debromination products ranging from hexa- to mono-BDEs in 90 days. The half-lives of BDE-153 in eight different sediments varied from 7.6 to 165 days, with higher debromination in mangrove than marine and fresh water pond sediments. All sediments exhibited the preference in removing the bromine in para, followed by meta, and the lowest in ortho positions; however, fresh water pond sediments had relatively higher fractions of meta (BDE-99) and ortho substitution (BDE118) of the three penta-BDE products. Mai Po mangrove and fresh water pond subsurface sediments were also capable of debrominating BDE-47 in 90 days of anaerobic incubation with half-lives of 76.2 and 56.9 days, respectively; but not BDE-209. BDE-47, -153, and -209 in Mai Po surface sediment were not transformed under 30 day aerobic incubation. This study demonstrated that the microbialmediated debromination of BDE-47 and -153 occurred in natural subsurface sediments under anaerobic conditions although the rates and pathways varied among the sediment types.



INTRODUCTION Polybrominated diphenyl ethers (PBDEs) are serious environmental pollutants because of their persistence and adverse effects on ecosystems and humans.1−3 Solid matrices, such as soil and sediment, are major sinks of PBDEs due to their strong hydrophobicity.4 High concentrations of PBDEs were found in sediment and soil around the world and the Pearl River Delta (PRD), especially in the “hot spots” near the recycling sites of electronic wastes (e-wastes).5,6 Previous studies of PBDEs focused mainly on their concentrations in different environmental compartments and their potential adverse health effects. Only a few studies reported the microbial transformation of PBDEs,7−11 which were mainly on their degradation in biological reactors/sewage sludge treatment processes,7,12 or by microbial consortia/isolates, such as Dehalococcoides, Sulf urospirillum, Burkholderia, Rhodococcus, Sphingomonas, and white rot fungi, in liquid media.8−10,13,14 Research on the debromination of PBDEs by the intrinsic microorganisms in sediments has been very limited, in spite of its importance in the natural attenuation potential of contaminated sediments. Lee and He15 found that octa-BDEs were reduced to products ranging from hexa- to nona-BDEs but at different rates in sediments collected from different locations in East Asia, © 2014 American Chemical Society

Southeast Asia, and North America under anaerobic conditions. Tokarz et al.11 reported that the microorganisms in freshwater sediment collected from Celery Bog Park, West Lafayette, IN (USA) could effectively degrade BDE-47 and -99 under anaerobic conditions, but the reductive debromination of BDE-209 was very slow, with a half-live over a decade. Schaefer and Flaggs16 did not observe any significant evidence on the anaerobic debromination of deca-BDE in sediments during a 32 week period. These results showed that debromination under anaerobic conditions varied among BDE congeners and sediment types. The river, marine, brackish, and estuarine (such as mangrove) sediments have different grain sizes, salinity, redox potential, concentrations of organic matter, nutrients, and anthropogenic pollutants, as well as microbial community structure, and would have different potentials in transforming pollutants. Wang et al.17 reported that intertidal mangrove sediments had more diverse and special bacterial communities than that found in fresh water reservoirs and Received: Revised: Accepted: Published: 4724

December 3, 2013 March 4, 2014 March 28, 2014 March 28, 2014 dx.doi.org/10.1021/es4053818 | Environ. Sci. Technol. 2014, 48, 4724−4731

Environmental Science & Technology

Article

marine sediments. Higher bacterial α-diversities were found in the sediments collected inside the mangrove forest (bulk and rhizosphere) than that of the outside (mudflat and edge) from the same mangrove swamp.18 Knowledge on PBDE biodegradation by the indigenous microorganisms in sediments under aerobic conditions is even more inadequate than that of anaerobic debromination. Only the lower brominated congeners such as mono- and di-BDE could be degraded by some isolated bacterial or fungal strains under aerobic conditions,19,20 while most of the highly brominated congeners, such as tetra- and penta-BDEs, were not aerobically biotransformed. The present study aims to compare the debromination potentials of three PBDE congeners by the indigenous microorganisms in different types of sediments, including mangrove, fresh water pond, and marine, collected from Hong Kong Special Administrative Region (SAR). The study also attempts to determine the debromination products of PBDEs in these sediments. BDE-47, BDE-153, and BDE-209 having 4, 6, and 10 bromine atoms, respectively, were chosen to represent low, medium, and high brominated BDE congeners. BDE-209 had the highest concentrations in mangrove sediments in SAR, BDE-153 was the second predominant congener,21 and BDE-47 was one of the most prevalent and toxic congeners.22

Ehrenstorfer (purity > 99%), respectively. The 1% impurities in PBDE standard solutions could be neglected because the debromination products were in very small amounts ( 30 ppt. Aerobic Transformation of PBDEs in Mai Po Sediment Slurry. The percentages of residual BDE-47, -153, and -209 in the surface sediment slurry of Mai Po did not show any significant changes during the 30 day aerobic incubation

BDE-153 could be debrominated to three penta-BDE congeners: (i) BDE-99 by meta substitution, (ii) BDE-101 by para substitution, and (iii) BDE-118 by ortho substitution. The fractions of BDE-101 to all three penta-BDE products were the highest while that of the BDE-118 were the lowest (Table 1), suggesting that all sediments exhibited the preference in removing para bromine to form BDE-101, while the debromination through ortho bromine was difficult. However, the debromination pathways of BDE-153 between saline and nonsaline sediments might be different. All saline sediments had more than 94% BDE-101 and less than 1% BDE-118. On the other hand, the fractions of BDE-101 in fresh water pond sediments (NSWf and MPf) were significantly lower but those of BDE-118 were higher than that in saline sediments (Table 1). Not only BDE-118 caused the changes in the metabolite profile, the range of BDE-99 also varied among sediment types, with significantly higher values in fresh water pond than marine and mangrove sediments. It is possible that the microorganisms responsible for the debromination of PBDEs in saline sediments were different from that in fresh water pond sediments, and the latter sediments might have higher abilities to remove the relatively more difficult ortho bromine in BDE153. Anaerobic Debromination of BDE-209 in Sediment Slurry. The percentages of residual BDE-209 to initial spiked concentrations in both MPm and MPf sediment slurries did not 4728

dx.doi.org/10.1021/es4053818 | Environ. Sci. Technol. 2014, 48, 4724−4731

Environmental Science & Technology

Article

Table 1. Fractions of the Products of BDE-153 with One-Bromine Removed at the End of 90 days of Anaerobic Incubation in Different Sediment Slurries (Calculated According to the Peak Area of Each Congener to Total Areas of Three Penta-BDEs Identified in GC/MS Chromatograms; Mean and Standard Deviation of Three Replicates Shown) penta-BDEs BDE-99 mangrove sediments

fresh water pond sediments marine sediment

MPm STKm HCm TKm TOm MPf NSWf SKo

0.91 4.67 2.63 1.86 5.08 6.11 9.38 3.11

± ± ± ± ± ± ± ±

0.05 1.00 0.22 0.17 0.43 0.79 0.85 0.40

BDE-101

BDE-118

± ± ± ± ± ± ± ±

0.27 ± 0.03 0.85 ± 0.03 0.71 ± 0.01 0.96 ± 0.12 0.64 ± 0.08 22.1 ± 11.5 3.54 ± 0.78 0.41 ± 0.02

98.8 94.5 96.7 97.2 94.3 71.8 87.1 96.5

0.02 0.97 0.23 0.25 0.42 11.8 0.23 0.37

Table 2. Biodegradation Rates (k, day−1) and Half-Lives (t1/2, days) of BDE-47 and BDE-153 in Anaerobic Sediment Slurries (r2, Correlation Coefficient of the First-Order Rate Model) BDE-47 BDE-153

mangrove sediment fresh water pond sediment mangrove sediments

fresh water pond sediments marine sediment

MPm MPf MPm STKm HCm TKm TOm MPf NSWf SKo

k

t1/2

r2

0.009 0.013 0.017 0.091 0.015 0.033 0.066 0.004 0.012 0.015

76.2 52.9 41.3 7.6 46.8 21.1 10.5 165.0 59.8 47.8

0.95 0.89 0.99 0.99 0.998 0.91 0.99 0.87 0.96 0.94

BDE-209 were more persistent than the lower ones and a longer incubation time is needed in future studies. BDE-153 in this study was first debrominated to three penta-BDE congeners; the removal of bromine at the para position was the most preferred while the ortho bromine was the most difficult to remove (Table 1). Robrock et al.9 also showed that all three tested dehalogenating cultures preferentially removed the bromine in the para position in the rings of PBDEs, while the ortho substitution products were minor and only one culture could debrominate BDE-153 and BDE-47 by ortho substitution to BDE-118 and BDE-28, respectively. It is possible that BDE-101 is more stable and recalcitrant than BDE-99 and BDE-118 based on their chemical structure and the position of bromine atoms. It has been suggested that steric hindrance may probably be the cause of why the ortho debromination product BDE-118 was only in a minor abundance.25 However, this needs to be confirmed by spiking each of these three congeners to the sediments and following the debromination rate of each congener in future research. Intrinsic Debromination Abilities of Different Sediments. Sediments, important sinks for persistent organohalogen pollutants, are often anaerobic and provide an environment for them to undergo reductive dehalogenation.33,35,37 Until now, studies on the intrinsic microbial debromination of PBDEs in sediments were limited, as most of the previous research was conducted using the microbial extracted culture or pure strains in liquid media.7,11,36,38 The biodegradation of PBDEs in liquid media would not be the same as in sediment as the availability of PBDEs to microorganisms is often higher in liquid media than in contaminated soil/sediment. In the present study, different types of sediments, although all collected from Hong Kong SAR, a city with an area of 1000 km2, showed different PBDE

(Supporting Information Figure S2). No new peak in the GC/ MS chromatogram was found, indicating that the parent PBDEs spiked in the sediment slurry did not undergo any transformation or degradation in 30 days.



DISCUSSION Debromination of PBDEs in Sediment Slurries under Aerobic and Anaerobic Conditions. In the present study, the three tested PBDE congeners (tetra-, hexa-, and decaBDEs) still remained at the same levels at the end of 30 days of aerobic incubation, suggesting that microbial transformations of these three congeners were not significant. However, microorganisms, particularly bacteria, having evolved several strategies for the dehalogenation and degradation of haloorganic compounds such as PCBs32,33 and PBDEs with six or fewer bromines, could be transformed by bacterial strains or a mixed culture in liquid media.10,13 More research is needed to understand the intrinsic aerobic degradation process in sediments. Reductive dehalogenation was the predominant process responsible for the initial degradation of organo-halides, PCBs, and polybrominated biphenyls (PBBs) in anaerobic sediments.33−35 However, during 90 days of anaerobic incubation, the concentration of the spiked BDE-209 remained the same while BDE-47 and -153 were debrominated with the formation of lower brominated congeners. Shin et al.36 also found that the concentrations of BDE-47, -99, and -100 decreased by 22−35.6%, whereas the levels of BDE-138, -153, -154, and -180 remained stable during the 328 day incubation in municipal sewage. The half-life of BDE-209 in anaerobic sediment was reported to be well over a decade.11 The severely low bioavailability and high persistence of BDE-209 in sediment might explain the slow debromination process. These suggested that highly brominated congeners such as 4729

dx.doi.org/10.1021/es4053818 | Environ. Sci. Technol. 2014, 48, 4724−4731

Environmental Science & Technology

Article

under anaerobic conditions was the dominant process in this study, which is particularly important for mangrove sediments. The mangrove swamps in tropical and subtropical regions are subject to tidal flushing, with only the surface sediment of 0−2 cm being aerobic and the majority of the sediments being anaerobic.39 These results indicated the significance of natural attenuation in contaminated mangrove sediments and the potential of using the enriched debrominating microorganisms from mangrove sediments for bioremediation purposes.

debromination abilities. Mangrove sediment slurries generally had higher BDE-153 debromination abilities than marine and fresh water pond sediments. On the contrary, the fresh water pond sediment had a higher BDE-47 debromination ability than the mangrove sediment, both collected from the Mai Po RAMSAR area. Lee and He15 also found that the microorganisms in sediments or soils collected from 28 different locations showed different abilities to debrominate PBDEs. Not only debromination rates, the relative abundance of the daughter congeners produced during debromination was also different among sediment types in the present study. It is possible that the indigenous microorganisms in sediments are different leading to variations in debromination abilities and pathways among sediment types, as well as congeners. Wang et al.17 reported that intertidal mangrove sediments had more diverse and special bacterial communities than that in fresh water reservoirs and marine sediments. Even within the same mangrove swamp, Mai Po, higher bacterial α-diversities were found in the sediments collected inside the mangrove forest (bulk and rhizosphere) than those outside (mudflat and edge), and actinobacteria, acidobacteria, nitrospirae and verrucomicrobia were enriched from the inside mangrove sediment while proteobacteria and deferribacteres were more dominant in the sediments collected outside of the mangrove.18 Zeng et al.25 also found that the proportion of BDE-99 and -101 produced from the microbial debromination of BDE-153 differed between the enriched cultures, as each culture had different debrominating bacterial strains. The microbial communities in sediment also depend on sediment properties, including grain size, salinity, and redox potential, concentrations of organic matter, nutrients, and anthropogenic pollutants. The mangrove sediment in Mai Po was more saline and had higher total organic matter content than the fresh water pond sediment, which may also lead to different microbial diversities and dominant species. Higher content of TOM could retain more PBDEs in the sediment and reduce their bioavailability to microorganisms leading to different debromination potentials between sediment types. A high, positive correlation (R2 = 0.82) was found between the half-lives of BDE-153 and the TOM content in mangrove sediments but the fresh water pond and marine sediments did not follow the same trend (Supporting Information Figure S3). This is the first study comparing the debromination abilities and pathways of PBDEs in different sediments in Hong Kong SAR under aerobic and anaerobic conditions. The aerobic biodegradation, biotransformation, or debromination of the highly brominated BDE congeners, including BDE-47, -153, and -209, in Mai Po mangrove sediment, were more difficult than the anaerobic processes, and deserve more research in the future. On the other hand, all subsurface sediments, including mangrove, fresh water pond, and marine, could debrominate BDE-153 under anaerobic conditions although mangrove sediments had higher debromination potentials in general. BDE-47 could also be debrominated by mangrove and fresh water pond sediments, but the former sediment had a lower rate. It is possible that the debrominating microorganisms are widespread in anaerobic sediments, but the dominant bacterial groups responsible for the debromination of different congeners varied among sediment types. Further investigations are needed to investigate the microbial communities in different sediments, their changes during debromination of PBDEs, and their roles in the debromination of PBDEs under anaerobic conditions. The reductively debromination of BDE-47 and -153



ASSOCIATED CONTENT

S Supporting Information *

Tables listing characteristics of collected sediments and percentages of the peak areas of specific cogeners compared to the total peak areas of all cogeners in different sediment slurries and figures showing the percent changes of residual BDE-209, BDE-47, and BDE-153 to the initial spiked concentrations in slurries and regression analysis for the halflife results from BDE-153 and TOM content in slurries. This material is available free of charge via the Internet at http:// pubs.acs.org.



AUTHOR INFORMATION

Corresponding Author

*Phone: +852-34427793; fax: +852-34420522; e-mail: [email protected]. Notes

The authors declare no competing financial interest.



ACKNOWLEDGMENTS The present study was supported by the research fund from the State Key Laboratory in Marine Pollution, City University of Hong Kong and the Science, Technology and Innovation Committee of the Shenzhen Municipality, China.



REFERENCES

(1) McDonald, T. A. A perspective on the potential health risks of PBDEs (DIOXIN 2000 Conference, Monterey, CA, USA). Chemosphere 2002, 46, 745−755. (2) Meerts, I.; Letcher, R. J.; Hoving, S.; Marsh, G.; Bergman, A.; Lemmen, J. G. In vitro estrogenicity of polybrominated diphenyl ethers, hydroxylated PBDEs, and polybrominated bisphenol A compounds. Environ. Health Perspect. 2001, 109, 399−407. (3) Costa, L. G.; Giordano, G. Developmental neurotoxicity of polybrominated diphenyl ether (PBDE) flame retardants. Neurotoxicology 2007, 28, 1047−1067. (4) Rahman, F.; Langford, K. H.; Scrimshaw, M. D.; Lester, J. N. Polybrominated diphenyl ether (PBDE) flame retardants. Sci. Total Environ. 2001, 275, 1−17. (5) Wang, D. L.; Cai, Z. W.; Jiang, G. B.; Leung, A.; Wong, M. H.; Wong, W. K. Determination of polybrominated diphenyl ethers in soil and sediment from an electronic waste recycling facility. Chemosphere 2005, 60, 810−816. (6) Luo, Y.; Luo, X. J.; Lin, Z.; Chen, S. J.; Liu, J.; Mai, B. X.; Yang, Z. Y. Polybrominated diphenyl ethers in road and farmland soils from an e-waste recycling region in Southern China: Concentrations, source profiles, and potential dispersion and deposition. Sci. Total Environ. 2009, 407, 1105−1113. (7) Gerecke, A. C.; Hartmann, P. C.; Heeb, N. V.; Kohler, H. P. E.; Giger, W.; Schmid, P.; Zennegg, M.; Kohler, M. Anaerobic degradation of decabromodiphenyl ether. Environ. Sci. Technol. 2005, 39, 1078−1083. (8) He, J. Z.; Robrock, K. R.; Alvarez-Cohen, L. Microbial reductive debromination of polybrominated diphenyl ethers (PBDEs). Environ. Sci. Technol. 2006, 40, 4429−4434.

4730

dx.doi.org/10.1021/es4053818 | Environ. Sci. Technol. 2014, 48, 4724−4731

Environmental Science & Technology

Article

(9) Robrock, K. R.; Korytar, P.; Alvarez-Cohen, L. Pathways for the anaerobic microbial debromination of polybrominated diphenyl ethers. Environ. Sci. Technol. 2008, 42, 2845−2852. (10) Robrock, K. R.; Coelhan, M.; Sedlak, D. L.; Alvarez-Cohent, L. Aerobic biotransformation of polybrominated diphenyl ethers (PBDEs) by bacterial isolates. Environ. Sci. Technol. 2009, 43, 5705− 5711. (11) Tokarz, J. A.; Ahn, M. Y.; Leng, J.; Filley, T. R.; Nies, L. Reductive debromination of polybrominated diphenyl ethers in anaerobic sediment and a biominetic system. Environ. Sci. Technol. 2008, 42, 1157−1164. (12) Rayne, S.; Ikonomou, M. G.; Antcliffe, B. Rapidly increasing polybrominated diphenyl ether concentrations in the Columbia River system from 1992 to 2000. Environ. Sci. Technol. 2003, 37, 2847−2854. (13) Kim, Y. M.; Nam, I. H.; Murugesan, K.; Schmidt, S.; Crowley, D. E.; Chang, Y. S. Biodegradation of diphenyl ether and transformation of selected brominated congeners by Sphingomonas sp PH-07. Appl. Microbiol. Biot. 2007, 77, 187−194. (14) Yen, J. H.; Liao, W. C.; Chen, W. C.; Wang, Y. S. Interaction of polybrominated diphenyl ethers (PBDEs) with anaerobic mixed bacterial cultures isolated from river sediment. J. Hazard. Mater. 2009, 165, 518−524. (15) Lee, L. K.; He, J. Reductive debromination of polybrominated diphenyl ethers by anaerobic bacteria from soils and sediments. Appl. Environ. Microbiol. 2010, 76, 794−802. (16) Schaefer, E. C.; Flaggs, R. S. Potential for biotransformation of radiolabelled decabromodiphenyl oxide (DBDPO) in anaerobic sediment, Amended report, Wildlife International Ltd., Project No. 439E-104; Wildlife International: Easton, MD, USA, 2001. (17) Wang, Y.; Sheng, H. F.; He, Y.; Wu, J. Y.; Jiang, Y. X.; Tam, N. F. Y.; Zhou, H. W. Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of Illumina tags. Appl. Environ. Microbiol. 2012, 78, 8264−8271. (18) Jiang, X. T.; Peng, X.; Deng, G. H.; Sheng, H. F.; Wang, Y.; Zhou, H. W.; Tam, N. F. Y. Illumina sequencing of 16S rRNA tag revealed spatial variations of bacterial communities in a mangrove wetland. Microb. Ecol. 2013, 66, 96−104. (19) Schmidt, S.; Wittich, R. M.; Erdmann, D.; Wilkes, H.; Francke, W.; Fortnagel, P. Biodegradation of diphenyl ether and its monohalogenated derivatives by Sphingomonas sp. strain SS3. Appl. Environ. Microbiol. 1992, 58, 2744−2750. (20) Hundt, K.; Jonas, U.; Hammer, E.; Schauer, F. Transformation of diphenyl ethers by Trametes versicolor and characterization of ring cleavage products. Biodegradation 1999, 10, 279−286. (21) Zhu, H. W.; Wang, Y.; Wang, X. W.; Luan, T. G.; Tam, N. F. Y. Distribution and accumulation of polybrominated diphenyl ethers (PBDEs) in Hong Kong mangrove sediments. Sci. Total Environ. 2014, 468−469, 130−139. (22) Li, J.; Liu, X.; Yu, L. L.; Zhang, G.; Li, X. D.; Lee, C. S. L.; Lin, H. T. Comparing polybrominated diphenyl ethers (PBDEs) in airborne particles in Guangzhou and Hong Kong: Sources, seasonal variations and inland outflow. J. Environ. Monit. 2009, 11, 1185−1191. (23) Cambardella, C. A.; Gajda, A. M.; Doran, J. W.; Wienhold, B. J.; Kettler, T. A. Estimation of particulate and total organic matter by weight loss-on-ignition. In Assessment Methods for Soil Carbon; Lal, R., Kimble, J. M., Follett, R. F., Stewart, B. A., Eds; Lewis: Boca Raton, FL, USA. 2001; pp 349−359. (24) Li, C. H.; Wong, Y. S.; Tam, N. Y. F. Anaerobic biodegradation of polycyclic aromatic hydrocarbons with amendment of iron (III) in mangrove sediment slurry. Bioresour. Technol. 2010, 101, 8083−8092. (25) Zeng, X.; Massey Simonich, S. L.; Robrock, K. R.; Korytár, P.; Alvarez-Cohen, L.; Barofsky, D. F. Application of a congener-specific debromination model to study photodebromination, anaerobic microbial debromination, and Fe0 reduction of polybrominated diphenyl ethers. Environ. Toxicol. Chem. 2010, 29, 770−778. (26) Sanchez-Prado, L.; Lores, M.; Llompart, M.; Garcia-Jares, C.; Bayona, J. M.; Cela, R. Natural sunlight and sun simulator photolysis studies of tetra- to hexa-brominated diphenyl ethers in water using solid-phase microextraction. J. Chromatogr. A 2006, 1124, 157−166.

(27) Chen, S. J.; Gao, X. J.; Mai, B. X.; Chen, Z. M.; Luo, X. J.; Sheng, G. Y. Polybrominated diphenyl ethers in surface sediments of the Yangtze River Delta: Levels, distribution and potential hydrodynamic influence. Environ. Pollut. 2006, 144, 951−975. (28) Zou, M. Y.; Ran, Y.; Gong, J.; Maw, B. X.; Zeng, E. Y. Polybrominated diphenyl ethers in watershed soils of the Pearl River Delta, China: Occurrence, inventory, and fate. Environ. Sci. Technol. 2007, 41, 8262−8267. (29) Korytar, P.; Covaci, A.; de Boer, J.; Gelbin, A.; Brinkman, U. A. T. Retention-time database of 126 polybrominated diphenyl ether congeners and two Bromkal technical mixtures on seven capillary gas chromatographic columns. J. Chromatogr. A 2005, 1065, 239−249. (30) Stapleton, H. M.; Keller, J. M.; Schantz, M. M.; Kucklick, J. R.; Leigh, S. D.; Wise, S. A. Determination of polybrominated diphenyl ethers in environmental standard reference materials. Anal. Bioanal. Chem. 2007, 387, 2365−2379. (31) Zhu, H. W.; Wang, Y.; Tam, N. F. Y. Microcosm study on fate of polybrominated diphenyl ethers (PBDEs) in contaminated mangrove sediment. J. Hazard. Mater. 2014, 265, 61−68. (32) Fetzner, S. Bacterial dehalogenation. Appl. Microbiol. Biot. 1998, 50, 633−657. (33) Field, J. A.; Sierra-Alvarez, R. Microbial transformation and degradation of polychlorinated biphenyls. Environ. Pollut. 2008, 155, 1−12. (34) Smidt, H.; de Vos, W. M. Anaerobic microbial dehalogenation. Annu. Rev. Microbiol. 2004, 58, 43−73. (35) Morris, P. J.; Quensen, J. F., III; Tiedje, J. M.; Boyd, S. A. An assessment of the reductive debromination of polybrominated biphenyls in the Pine River Reservoir. Environ. Sci. Technol. 1993, 27, 1580−1586. (36) Shin, M.; Duncan, B.; Seto, P.; Falletta, P.; Lee, D. Y. Dynamics of selected pre-existing polybrominated diphenylethers (PBDEs) in municipal wastewater sludge under anaerobic conditions. Chemosphere 2010, 78, 1220−1224. (37) Mueller, K. E.; Mueller-Spitz, S. R.; Henry, H. F.; Vonderheide, A. P.; Soman, R. S.; Kinkle, B. K.; Shann, J. R. Fate of pentabrominated diphenyl ethers in soil: Abiotic sorption, plant uptake, and the impact of interspecific plant interactions. Environ. Sci. Technol. 2006, 40, 6662−6667. (38) Nyholm, J. R.; Lundberg, C.; Andersson, P. L. Biodegradation kinetics of selected brominated flame retardants in aerobic and anaerobic soil. Environ. Pollut. 2010, 158, 2235−2240. (39) Li, C. H.; Zhou, H. W.; Wong, Y. S.; Tam, N. Y. F. Vertical distribution and anaerobic biodegradation of polycyclic aromatic hydrocarbons in mangrove sediments in Hong Kong, South China. Sci. Total Environ. 2009, 407, 5772−5779.

4731

dx.doi.org/10.1021/es4053818 | Environ. Sci. Technol. 2014, 48, 4724−4731