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Microbial degradation of decabromodiphenyl ether (DBDE) in soil slurry microcosms

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Abstract

Decabromodiphenyl ether (DBDE), which has been identified as an endocrine disrupting compound, is used as brominated flame retardant, and this can result in serious bioaccumulation within ecological systems. The objective of this study was to explore DBDE bioremediation (25 mg/kg) using laboratory scale soil slurry microcosms. It was found that effective biodegradation of DBDE occurred in all microcosms. Various biometabolites were identified, namely polybrominated diphenyl ethers congeners and hydroxylated brominated diphenyl ether. Reductive debrominated products such as tri-BDE to hepta-BDE congeners were also detected, and their total concentrations ranged from 77.83 to 91.07 ng/g. The mechanism of DBDE biodegradation in soil slurry microcosms is proposed to consist of a series of biological reactions involving hydroxylation and debromination. Catechol 2,3-oxygenase genes, which are able to bring about meta-cleavage at specific unbrominated locations in carbon backbones, were identified as present during the DBDE biodegradation. No obvious effect on the ecological functional potential based on community-level physiological profiling was observed during DBDE biodegradation, and one major facultative Pseudomonas sp. (99 % similarity) was identified in the various soil slurry microcosms. These findings provide an important basis that should help environmental engineers to design future DBDE bioremediation systems that use a practical microcosm system. A bacterial-mixed culture can be selected as part of the bioaugmentation process for in situ DBDE bioremediation. A soil/water microcosm system can be successfully applied to carry out ex situ DBDE bioremediation.

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Abbreviations

AWCD:

Average well color development

CLPP:

Community-level physiological profiling

DBDE:

Decabromodiphenyl ether

DGGE:

Denaturing gradient gel electrophoresis

HBN:

High bromine number

HRMS:

High resolution mass spectrometer

LBN:

Low bromine number

MSB:

Inorganic salt growth medium

PBDE:

Polybrominated diphenyl ethers

PCA:

Principal component analysis

PDECD:

Pulsed discharge electron capture detector

POPs:

Persistent organic pollutants

SOM:

Soil organic matte

TCS:

Taichung natural soil

References

  • Albina ML, Alonso V, Linares V, Bellés M, Sirvent JJ, Domingo JL, Sánchez DL (2010) Effects of exposure to BDE-99 on oxidative status of liver and kidney in adult rats. Toxicology 271:51–56

    Article  CAS  Google Scholar 

  • Bǔnemann EK, Bossio DA, Smithson PC, Frossard E, Oberson A (2004) Microbial community composition and substrate use in a highly weathered soil as affected by crop rotation and P fertilization. Soil Biol Biochem 36:889–901

    Article  Google Scholar 

  • Chang Y-T, Lee J-F, Hung C-H (2007) PAH biodegradation in surfactant-water systems based on the theory of cohesive energy density (CED). J Chem Technol Biotechnol 82:442–452

    Article  CAS  Google Scholar 

  • Chen C, Zhao H, Chan J, Qiao X, Xie Q, Zhang Y (2012a) Polybrominated diphenyl ethers in soils of the modern Yellow River delta, China: occurrence, distribution and inventory. Chemosphere 88:791–797

    Article  CAS  Google Scholar 

  • Chen Q, Yu L, Yang L, Zhou B (2012b) Bioconcentration and metabolism of decabromodiphenyl ether (BDE-209) result in thyroid endocrine disruption in Zebrafish Larvae. Aquat Toxicol 110–111:141–148

    Article  Google Scholar 

  • Chou H-L, Chang Y-T, Liao Y-F, Lin C-H (2013) Biodegradation of decabromodiphenyl ether (BDE-209) by bacterial mixed cultures in a soil/water system. Int Biodeterior Biodegrad 85:671–682

    Article  CAS  Google Scholar 

  • Cincinelli A, Martellini T, Misuri L, Sweetman E, Laschi S, Palchetti I (2012) PBDEs in Italian sewage sludge and environmental risk of using sewage sludge for land application. Environ Pollut 161:229–234

    Article  CAS  Google Scholar 

  • Deng D, Guo J, Sun G, Chen X, Qiu M, Xu M (2011) Aerobic debromination of Deca-BDE: isolation and characterization of an indigenous isolate from a PBDE contaminated sediment. Int Biodeterior Biodegrad 65:465–469

    Article  CAS  Google Scholar 

  • Ding C, Chow WL, He J (2013) Isolation of Acetobacterium sp. strain AG, which reductively debrominates octa- and pentabrominated diphenyl ether technical mixtures. Appl Environ Microbiol 79:1110–1117

    Article  CAS  Google Scholar 

  • Fang HHP, Zhang T, Liu H (2002) Microbial diversity of a mesophilic hydrogen-producing sludge. Appl Microbiol Biotechnol 58:112–118

    Article  CAS  Google Scholar 

  • Fangstrom B, Hovander L, Bignert A, Athanassiadis I, Linderholm L, Grandjean P, Weihe P, Bergman A (2005) Concentrations of polybrominated diphenyl ethers, polychlorinated biphenyls, and polychlorobiphenylols in serum from pregnant faroese women and their children 7 years later. Environ Sci Technol 39:9457–9463

    Article  Google Scholar 

  • Frac M, Karolina O, Lipiec J (2012) Community level physiological profiles (CLPP), characterization and microbial activity of soil amended with diary sewage sludge. Sensors 12:3253–3268

    Article  Google Scholar 

  • Frederiksen M, Vorkamp K, Mathiesen L, Mose T, Knudsen LE (2010) Research placental transfer of the polybrominated diphenyl ethers BDE-47, BDE-99 and BDE-209 in a human placenta perfusion system: an experimental study. Environ Heal 9:32

    Article  Google Scholar 

  • Gerecke AC, Giger W, Hartmann PC, Heeb NV, Kohler H-PE, Schmid P, Zennegg M, Kohler M (2006) Anaerobic degradation of brominated flame retardants in sewage sludge. Chemosphere 64:311–317

    Article  CAS  Google Scholar 

  • Gevao B, Ghadban AN, Uddin S, Jaward FM, Bahloul M, Zafar J (2011) Polybrominated diphenyl ethers (PBDEs) in soils along a rural–urban-rural transect: sources, concentration gradients, and profiles. Environ Pollut 159:3666–3672

    Article  CAS  Google Scholar 

  • Kim Y-M, Nam I-H, Murugesan K, Schmidt S, Crowley DE, Chang Y-S (2007) Biodegradation of diphenyl ether and transformation of selected brominated congeners by Sphingomonas sp. PH-07. Appl Microbiol Biotechnol 77:187–194

    Article  CAS  Google Scholar 

  • Li Y, Lin T, Chen Y, Hu L, Guo Z, Zhang G (2012) Polybrominated diphenyl ethers (PBDEs) in sediments of the costal East China Sea: occurrence, distribution and mass inventory. Environ Pollut 171:156–161

    Article  Google Scholar 

  • Liang SX, Gao HX, Zhao YY, Ma XM, Sun HW (2010) Effects of repeated exposure to decabrominated diphenyl Ether (BDE-209) on mice nervous system and its self-repair. Environ Toxicol Pharmacol 29:297–301

    Article  CAS  Google Scholar 

  • Liu L, Zhu W, Xiao L, Yang L (2011) Effect of decabromodiphenyl ether (BDE 209) and dibromodiphenyl ether (BDE 15) on soil microbial activity and bacterial community composition. J Hazard Mater 186:883–890

    Article  CAS  Google Scholar 

  • Mackay D, Shiu WY, Ma K-C, Lee SC (2006) Handbook of physical-chemical properties and environmental fate for organic chemicals. Volume II-Halogenated Hydrocarbons, 2nd edn. CRC Press, Taylor & Francis Group, FL

    Google Scholar 

  • Moon HB, Choi M, Yu J, Jung RH, Choi HG (2012) Contamination and potential sources of polybrominated diphenyl ethers (PBDEs) in water and sediment from the artificial lake Shihwa, Korea. Chemosphere 88:837–843

    Article  CAS  Google Scholar 

  • Nyholm JR, Lundberg C, Andersson PL (2010) Biodegradation kinetics of selected brominated flame retardants in aerobic and anaerobic soil. Environ Pollut 158:2235–2240

    Article  CAS  Google Scholar 

  • Pfeifer F, Trüper HG, Klein J, Schacht S (1993) Degradation of diphenyl ether by Pseudomonas cepacia Et4: enzymatic release of phenol from 2, 3-dihydroxydiphenyl ether. Arch Microbiol 159:323–329

    Article  CAS  Google Scholar 

  • Qiu M, Chen X, Deng D, Guo J, Sun G, Mai B, Xu M (2012) Effects of electron donors on anaerobic microbial debromination of polybrominated diphenyl ethers (PBDEs). Biodegradation 23:351–361

    Article  CAS  Google Scholar 

  • Robrock KR, Coelhan M, Sedlak DL, Alvarez-Cohen L (2009) Aerobic biotransformation of polybrominated diphenyl ethers (PBDEs) by bacterial isolates. Environ Sci Technol 43:5705–5711

    Article  CAS  Google Scholar 

  • Robrock KR, Mohn WW, Eltis LD, Alvarez-Cohen L (2011) Biophenyl and ethylbenzene dioxygenases of Rhodococcus jostii RHA1 transform PBDEs. Biotechnol Bioeng 108:313–314

    Article  CAS  Google Scholar 

  • Saegusa Y, Fujimoto H, Woo GH, Ohishi T, Wang L, Mitsumori K, Nishikawa A, Shibutani M (2012) Transient aberration of neuronal development in the hippocampal dentate gyrus after developmental exposure to brominated flame retardants in rats. Arch Toxicol 86:1431–1442

    Article  CAS  Google Scholar 

  • Shao J, White CC, Dabrowski MJ, Kavanagh TJ, Eckert ML, Gallagher EP (2008) The role of mitochondrial and oxidative injury in BDE 47 toxicity to human fetal liver hematopoietic stem cells. Toxicol Sci 101:81–90

    Article  CAS  Google Scholar 

  • Shi G, Yin H, Ye J, Peng H, Li J, Luo C (2013) Aerobic biotransformation of decabromodiphenyl ether (PBDE-209) by Pseudomonas aeruginosa. Chemosphere 93:1487–1493

    Article  CAS  Google Scholar 

  • Stiborova H, Vrkoslavova J, Lovecka P, Pulkrabova J, Hradkova P, Hajslova J, Demnerova K, Stiborova (2015) Aerobic biodegradation of selected polybrominated diphenyl ethers (PBDEs) in wastewater sewage sludge. Chemosphere 118:315–321

    Article  CAS  Google Scholar 

  • Tokarz JA, Ahn MY, Leng J, Filley TR, Nies L (2008) Reductive debromination of polybrominated diphenyl ethers in anaerobic sediment and a biomimetic system. Environ Sci Technol 42:1157–1164

    Article  CAS  Google Scholar 

  • Toms L-ML, Mortimer M, Symons RK, Paepke O, Mueller JF (2008) Poly-brominated diphenyl ethers (PBDEs) in sediments by salinity and land-use type from Australia. Environ Int 34:58–66

    Article  CAS  Google Scholar 

  • U.S. EPA (2008) (Environmental Protection Agency), Toxicological review of decabromodipheny ether (BDE-209), EPA/635/R-07/008F, Washington DC

  • Viberg H, Fredriksson A, Jakobsson E, Orn U, Eriksson P (2003) Neurobehavioral derangements in adult mice receiving decabrominated diphenyl ether (PBDE 209) during a defined period of neonatal brain development. Toxicol Sci 76:112–120

    Article  CAS  Google Scholar 

  • Vonderheide AP, Mueller-Spitz SR, Meija J, Welsh GL, Mueller KE, Kinkle BK, Shanna JR, Caruso JA (2006) Rapid breakdown of brominated flame retardants by soil microorganisms. J Anal At Spectrom 21:1232–1239

    Article  CAS  Google Scholar 

  • Wang P, Zhang Q-H, Wang T, Chen W-H, Ren D-W, Li Y-M, Jiang G-B (2012) PCBs and PBDEs in environmental samples from King George Island and Ardley Island Antarctica. RSC Adv 2:1350–1355

    Article  CAS  Google Scholar 

  • Wei HA, Aziz-Schwanbeck C, Zou Y, Corcoran MB, Poghosyan A, Li A, Rockne KJ, Christensen ER, Sturchio NC (2012) Polybromodiphenyl ethers and decabromodiphenyl ethane in aquatic sediments from southern and eastern Arkansas. U.S.A. Environ Sci Technol 46:8017–8024

    Article  CAS  Google Scholar 

  • Xia X (2013) Microbial degradation of polybrominated diphenyl ethers: current and future. J Bioremed Biodeg 4:e130

    Article  Google Scholar 

  • Yang C-W, Huang H-W, Chao W-L, Chang B-V (2015) Bacterial communities associated with aerobic degradation of polybrominated diphenyl ethers from river sediments. Environ Sci Pollut Res 22:3810–3819

    Article  CAS  Google Scholar 

  • Yen JH, Liao WC, Chen WC, Wang YS (2009) Interaction of polybrominated diphenyl ethers (PBDEs) with anaerobic mixed bacterial cultures isolated from river sediment. J Hazard Mater 165:518–524

    Article  CAS  Google Scholar 

  • Yogui GT, Sericano JL (2009) Polybrominated diphenyl ether flame retardants in the U.S. marine environment: a review. Environ Int 35:655–666

    Article  CAS  Google Scholar 

  • Zhang S, Xia X, Xia N, Wu S, Gao F, Zhou W (2013) Identification and biodegradation efficiency of a newly isolated 2, 2’, 4, 4’-tetrabromodiphenyl ether (BDE-47) aerobic degrading bacterial strain. Int Biodeterior Biodegrad 76:24–31

    Article  CAS  Google Scholar 

  • Zhu W, Liu L, Zou P, Xiao L (2010) Effect of decabromodiphenyl ether (BDE 209) on soil microbial activity and bacterial community composition. World J Microbiol Biotechnol 26:1891–1899

    Article  Google Scholar 

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Acknowledgments

The financial support for this study was provided by the Ministry of Science and Technology (previously National Science Council), Taiwan, and this is gratefully acknowledged. The project numbers are NSC99-2627-B- 031–002 and MOST102-2221-E-031-001-MY2. Part of the results/discussions was presented at the 1st International Conference on Emerging Contaminants, Kaohsiung, in Taiwan on October, 2013. The authors thank Mrs. Liao, Yi-Fen for her great efforts during the experiments.

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Correspondence to Yi-Tang Chang.

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Responsible editor: Philippe Garrigues

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Chou, HL., Hwa, MY., Lee, YC. et al. Microbial degradation of decabromodiphenyl ether (DBDE) in soil slurry microcosms. Environ Sci Pollut Res 23, 5255–5267 (2016). https://doi.org/10.1007/s11356-015-5767-x

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