Biodegradation of decabromodiphenyl ether (BDE-209) by bacterial mixed cultures in a soil/water system

International Biodeterioration and Biodegradation

Volumn 85, Issue , 2013, Pages 671-682

  Chou, Hsi Ling ^a   Chang, Yi Tang ^a   Liao, Yi Fen ^a   Lin, Ching Hsing ^b  

^a SOOCHOW UNIVERSITY   (Taiwan)

^b National Taitung College   (Taiwan)

Author keywords

Debromination; Decabromodiphenyl ether (DBDE); Nitrification denitrification; UV irradiation

Indexed keywords

AEROBIC BIODEGRADATION; BROMINATED FLAME RETARDANTS; DEBROMINATION; DECABROMODIPHENYL ETHERS; DECABROMODIPHENYL ETHERS (BDE209); MIXED BACTERIAL CULTURE; NITRIFICATION-DENITRIFICATION; UV IRRADIATION;

BIOCHEMISTRY; ETHERS; HEALTH RISKS; MICROBIOLOGY; ORGANIC POLLUTANTS; PHOTODEGRADATION; PHOTOLYSIS; RATE CONSTANTS;

BIODEGRADATION;

BACTERIUM; BIOACCUMULATION; BIODEGRADATION; CONCENTRATION (COMPOSITION); DENITRIFICATION; ETHER; HEALTH RISK; PBDE; PHOTOLYSIS; SOIL POLLUTION; SORPTION; WATER POLLUTION;

BACTERIA (MICROORGANISMS);

EID: 84886254915     PISSN: 09648305     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibiod.2013.05.006     Document Type: Article

References (76)

1. Akutsu K., Takatori S., Nozawa S., Yoshiike M., Nakazawa H., Hayakawa K. Polybrominated diphenyl ethers in human serum and sperm quality. Bull. Environ. Contam. Toxicol. 2008, 80:345-350.
2. Altschul S.F. Basic local alignment search tool. J.Mol. Biol. 1990, 215:403-410.
3. Arrage A.A., Phelps T.J., Benoit R.E., White D.C. Survival of subsurface microorganisms exposed to UV radiation and hydrogen peroxide. Appl. Environ. Microbiol. 1993, 59:3545-3550.
4. Bader R., Leisinger T. Isolation and characterization of the Methylophilus sp. strain DMII gene encoding dichloromethane dehalogenase/glutathione s-transferase. J.Bacteriol. 1994, 3466-3473.
5. Baxter J., Cummings S.P. The degradation of the herbicide bromoxynil and its impact on bacterial diversity in a top soil. J.Appl. Microbiol. 2008, 104:1605-1616.
6. Cai T., Qian L., Cai S., Chen L. Biodegradation of benazolin-ethyl by strain Methyloversatilis sp. cd-1 isolated from activated sludge. Curr. Microbiol. 2011, 62:570-577.
7. Chen S.J., Tian M., Luo Y., Lin Z., Luo X.J., Mai B.X. Vertical profile of polybrominated diphenyl ethers (PBDEs) in sediment from an e-waste area in South China. Environ. Sci. 2010, 31:3088-3092. (in Chinese).
8. Charboneau J.P., Koger S.M. Plastics, pesticides and PBDEs: endocrine disruption and developmental disabilities. J.Dev. Phys. Disabil. 2008, 20:115-128.
9. Ciani A., Goss K.-U., Suchwarzenbach R.P. Light penetration in soil and particulate minerals. Eur. J. Soil. Sci. 2005, 56:561-574.
10. Cincinelli A., Martellini T., Misuri L., Lanciotti E., Sweetman A., Laschi S., Palchetti I. PBDEs in Italian sewage sludge and environmental risk of using sewage sludge for land application. Environ. Pollut. 2012, 161:229-234.
11. Public Health Statement for Polybrominated Diphenyl Ethers (PBDEs) 2004, CDC, CDC.
12. Darnerud P.O., Eriksen G.S., Jöhannesson T., Larsen P.B., Viluksela M. Polybrominated diphenyl ethers: occurrence, dietary exposure, and toxicology. Environ. Health Perspect. 2001, 109:49-68.
13. Darnerud P.O. Brominated flame retardants as possible endocrine disrupters. Int. J. Androl. 2008, 31:152-160.
14. Daum M., Zimmer W., Papen H., Kloos K., Nawrath K., Bothe H. Physiological and molecular biological characterization of ammonia oxidation of the heterotrophic nitrifier Pseudomonas putida. Curr. Microbiol. 1998, 37:281-288.
15. de Wit C.A. An overview of brominated flame retardants in the environment. Chemosphere 2002, 46:583-674.
16. Deng D., Guo J., Sun G., Chen X., Qiu M., Xu M. Aerobic debromination of deca-BDE: isolation and characterization of an indigenous isolate from a PBDE contaminated sediment. Int. Biodeterior. Biodegrad. 2011, 65:465-469.
17. Duhamel M., Wehr S., Yu L., Rizvi H., Seepersad D., Dworatzek S., Cox E.E., Edwards E.A. Comparison of anaerobic dechlorinating enrichment cultures maintained on tetrachloroethene, trichloroethene, cis-1,2-dichloroethene and vinyl chloride. Water Res. 2002, 36:4193-4202.
18. Doris K.-S., Thomas L. Dichloromethane dehalogenase of Hyphomicrobium sp. strain DM2. J.Bacteriol. 1985, 162:676-681.
19. Elkarmi A., Abu-Elteen K., Khader M. Modeling the biodegradation efficiency and growth of Pseudomonas alcaligenes utilizing 2,4-dichlorophenol as a carbon source Pre- and Post-exposure to UV radiation. Jordan J. Biol. Sci. 2008, 1:7-11.
20. Eriksson J., Green N., Marsh G., Bergman A. Photochemical decomposition of 15 polybrominated diphenyl ether congeners in methanol/water. Environ. Sci. Technol. 2004, 38:3119-3125.
21. Fang H.H.P., Zhang T., Liu H. Microbial diversity of a mesophilic hydrogen-producing sludge. Appl. Microbiol. Biotechnol. 2002, 58:112-118.
22. Fangstrom B., Hovander L., Bignert A., Athanassiadis I., Linderholm L., Grandjean P., Weihe P., Bergman A. Concentrations of polybrominated diphenyl ethers, polychlorinated biphenyls, and polychlorobiphenylols in serum from pregnant faroese women and their children 7 years later. Environ. Sci. Technol. 2005, 39:9457-9463.
23. Gerecke A.C., Hartsann P.C., Heeb N.V., Kohler H.P., Giger W., Schmid P., Zennegg M., Kohler M. Anaerobic degradation of decabromodiphenyl Ether. Environ. Sci. Technol. 2005, 39:1078-1083.
24. Gevao B., Ghadban A.N., Uddin S., Jaward F.M., Bahloul M., Zafar J. Polybrominated diphenyl ethers (PBDEs) in soils along a rural-urban-rural transect: sources, concentration gradients, and profiles. Environ. Pollut. 2011, 159:3666-3672.
25. Han S.-K., Bilski P., Karriker B., Sik R.H., Chignell C.F. Oxidation of flame retardant tetrabromobisphenol A by singlet oxygen. Environ. Sci. Technol. 2008, 42:166-172.
26. Hale R.C., Alaee M., Manchester-Neesvig J.B., Stapleton H.M., Ikonomou M.G. Polybrominated diphenyl ether flame retardants in the North American environment. Environ. Int. 2003, 29:771-779.
27. He J.K., Robrock R., Alvarez-Cohen L. Microbial reductive debromination of polybrominated diphenyl ethers (PBDEs). Environ. Sci. Technol. 2006, 40:4429-4434.
28. Herbstman J.B., Sjodin A., Apelberg B.J., Witter F.R., Halden R.U., Patterson D.G. Birth delivery mode modifies the associations between prenatal polychlorinated biphenyl (PCB) and polybrominated diphenyl ether (PBDE) and neonatal thyroid hormone levels. Environ. Health. Perspect. 2008, 116:1376-1382.
29. Hu T.L., Kung K.T. Study of heterotrophic nitrifying bacteria from waste water treatment systems treating acrylonitrile, butadiene and styrene resin waste water. Water Sci. Technol. 2000, 42:315-321.
30. Hengge-Aronis R., Lange R., Henneberg N., Fischer D. Osmotic regulation of rpoS-dependent genes in Escherichia coli. J.Bacteriol. 1993, 175:259-265.
31. Kapley A., Purohit H.J. Diagnosis of treatment efficiency in industrial wastewater treatment plants: a case study at a refinery ETP. Environ. Sci. Technol. 2009, 43:3789-3795.
32. 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. Biotechnol. 2007, 77:187-194.
33. Kim J.K., Park K.J., Cho K.S., Nam S.-W., Park T.-J., Bajpai R. Aerobic nitrification-denitrification by heterotrophic Bacillus strains. Bioresour. Technol. 2005, 96:1897-1906.
34. Kimbara K., Hashimoto T., Fukuda M., Koana T., Takagi M., Oishi M., Yano K. Isolation and characterization of a mixed culture that degrades polychlorinated biphenyls. Agri. Biol. Chem. 1988, 52:2885-2891.
35. Kiyohara H., Hatta T., Ogawa Y., Kakuda T., Yokoyama H., Takizawa N. Isolation of Pseudomonas pickettii strains that degrade 2,4,6-trichlorophenol and their dechlorination of chlorophenols. Appl. Environ. Microbiol. 1992, 58:1276-1283.
36. Lambo A.J., Patel T.R. Cometabolic degradation of polychlorinated biphenyls at low temperature by psychrotolerant bacterium Hydrogenophaga sp. IA3-A. Curr. Microbiol. 2006, 53:48-52.
37. Langford K., Scrimshaw M., Lester J. The impact of process variables on the removal of PBDEs and NPEOs during simulated activated sludge treatment. Arch. Environ. Contam. Toxicol. 2007, 54:1-7.
38. Liu L., Zhu W., Xiao L., Yang Liu Effect of decabromodiphenyl ether (BDE 209) and dibromodiphenyl ether (BDE 15) on soil microbial activity and bacterial community composition. J.Hazard. Mater. 2011, 186:883-890.
39. Madigan M.T., Martinko J.M., Dunlap P.V., Clark D.P. Brock of Biology of Microorganisms 2009, Pearson Benjamin Cummings, San Francisco, USA. 12th ed.
40. Mai B., Chen S., Luo X., Chen L., Yang Q., Sheng G., Peng P., Fu J., Zeng E. Distribution of polybrominated diphenyl ethers in sediments of the Pearl River Delta and adjacent South China Sea. Environ. Sci. Technol. 2005, 39:3521-3527.
41. Mancini S.A., Hirschorn S.K., Elaner M., Lacrampe-Couloume G., Sleep B.E., Edwards E.A., Lollar B.S. Effect of trace element concentration on enzyme controlled stable isotope fractionation during aerobic biodegradation of toluene. Environ. Sci. Technol 2006, 40:7675-7681.
42. Marsolek M.D., Torres C.I., Hausner M., Rittmann B.E. Intimate coupling of photocatalysis and biodegradation in a photocatalytic circulating-bed biofilm reactor. Biotechnol. Bioeng. 2008, 101:83-92.
43. Miller R.V., Kokjohn T.A. General microbiology of recA. environmental and evolutionary significance. Ann. Rev. Microbiol. 1990, 44:365-394.
44. Meeker J.D., Johnson P.I., Camann D., Hauser R. Polybrominated diphenyl ether (PBDE) concentrations in house dust are related to hormone levels in men. Sci. Total Environ. 2009, 407:3425-3429.
45. Moharikar A., Kapley A., Purohit H.J. Detection of dioxygenase genes present in various activated sludge. Environ. Sci. Pollut. Res. Int. 2003, 10:373-378.
46. Mulet M., David Z., Nogales B., Bosch R., Lalucat J., García-Valdés E. Pseudomonas diversity in crude-oil-contaminated intertidal sand samples obtained after the Prestige oil spill. Appl. Environ. Microbiol. 2011, 77:1076-1085.
47. Norris T.B., McDermott T.R., Castenholz R.W. The long-term effects of UV exclusion on the microbial composition and photosynthetic competence of bacteria in hot-spring microbial mats. FEMS Microbiol. Lett. 2002, 39:193-209.
48. 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.
49. Polo M., Gomez-Noya C., Quintana J.B., Llompart M., Garcia-Jares C., Cela R. Development of a solid-phase microextraction gas chromatography/tandem mass spectrometry method for polybrominated diphenyl ethers and polybrominated biphenyls in water samples. Anal. Chem. 2004, 76:1054-1062.
50. Pornsunthorntawee O., Wongpanit P., Chavadej S., Abe M., Rujiravanit R. Structural and physicochemical characterization of crude biosurfactant produced by Pseudomonas aeruginosa SP4 isolated from petroleum-contaminated soil. Bioresour. Technol. 2008, 99:1589-1595.
51. Pfeifer F., Trüper H.G., Klein J., Schacht S. Degradation of diphenyl ether by Pseudomonas cepacia Et4: Enzymatic release of phenol from 2,3-dihydroxydiphenyl ether. Arch. Microbiol. 1993, 159:323-329.
52. Rashedi H., Jamshidi E., Assadi M.M., Bonakdarpour B. Isolation and production of biosurfactant from Pseudomonas aeruginosa isolated from Iranian southern wells oil. Int. J. Environ. Sci. Tech. 2005, 2:121-127.
53. Rayne S., Ikonomou M.G., Whale M.D. Anaerobic microbial and photochemical degradation of 4, 4'-dibromodiphenyl ether. Water Res. 2003, 37:551-560.
54. Reysenbach A.-L., Pace N.R. Reliable amplification of hyperthermophilic archaeal 16S rRNA genes by the polymerase chain reaction. Achaea: A Laboratory Manual V-Thermophiles 1995, 101-107. Cold Spring Harbor Laboratory Press, Cold Spring Harbor. F.T. Robb, A.R. Place (Eds.).
55. Robrock K.R., Mohn W.W., Eltis L.D., Alvarez-Cohen L. Biphenyl and ethylbenzene dioxygenases of Rhodococcus jostii RHA1 transform PBDEs. Biotechnol. Bioeng. 2011, 108:313-321.
56. Robrock K.R., Coelhan M., Sedlak D.L., Alvarez-Cohen L. Biodegradation of polybrominated diphenyl ethers by aerobic bacteria. Environ. Sci. Technol. 2009, 43:5705-5711.
57. Rotander A., van Bavel B., Polder A., Rigét F., Au{eth}unsson G.A., Gabrielsen G.W., Víkingsson G., Bloch D., Dam M. Polybrominated diphenyl ethers (PBDEs) in marine mammals from Arctic and North Atlantic regions, 1986-2009. Environ. Int. 2012, 40:102-109.
58. Schmidt S., Wittich R.M., Erdmann D., Wilkes H., Francke W., Fortnagel P. Biodegradation of diphenyl ether and its monohalogenated derivatives by strain SS3. Appl. Environ. Microbiol. 1992, 58:2744-2750.
59. Söderström G., Sellström U., de Wit C.A., Tysklind M. Photolytic debromination of decabromodiphenyl ether (BDE 209). Environ. Sci. Technol. 2004, 38:127-132.
60. Shih Y.-H., Wang C.-K. Photolytic degradation of polybromodiphenyl ethers under UV-lamp and solar irradiations. J.Hazard. Mater. 2009, 165:34-38.
61. Stourman N.V., Rose J.H., Vuilleumier S., Armstrong R.N. Catalytic mechanism of dichloromethane dehalogenase from Methylophilus sp. strain DM11. Biochemistry 2003, 42:11048-11056.
62. Suh Y.-W., Buettner G.R., Venkataraman S., Treimer S.E., Robertson L.W., Ludewig G. UVA/B-induced formation of free radicals from decabromodiphenyl ether. Environ. Sci. Technol. 2009, 43:2581-2588.
63. Sanchez-Prado L., Llompart M., Lores M. Investigation of photodegradation products generated after UV-irradiation of five polybrominated diphenyl ethers using photo solid-phase microextraction. J.Chromatogr. A. 2005, 1071:85-92.
64. Sjödin A., Patterson T.D.G., Tand T.A., Bergman T. Areview on human exposure to brominated flame retardants-particularly polybrominated diphenyl ethers. Environ. Int. 2003, 29:829-839.
65. Taiwan EPA, 2012. Investigation of the distribution of the toxic chemical substrates in Taiwan. Available from: (in Chinese). http://www.epa.gov.tw.
66. Tamer E., Hamid Z., Aly A.M., Ossama E.T., Bo M., Benoit G. Sequential UV biological degradation of chlorophenols. Chemosphere 2006, 63:277-284.
67. Toms L.-M.L., Mortimer M., Symons R.K., Paepke O., Mueller J.F. Polybrominated diphenyl ethers (PBDEs) in sediments by salinity and land-use type from Australia. Environ. Int. 2008, 34:58-66.
68. van den Tweel W.J.J., Kok J.B., de Bont J.A.M. Reductive dechlorination of 2,4-dichlorobenzoate to 4-chlorobenzoate and hydrolytic dehalogenation of 4-chloro-, 4-bromo-, and 4-iodobenzoate by Alcaligenes denitrificans NTB-1. Appl. Environ. Microbiol. 1987, 53:810-815.
69. Vuilleumier S., Nadalig T., Haque Ul M.F., Magdelenat G., Lajus A., Roselli S., Muller E.E.L., Gruffaz C., Barbe V., Médigue C., Bringel F. Complete genome sequence of the chloromethane-degrading Hyphomicrobium sp. Strain MC1. J.Bacteriol. 2011, 193:5035-5036.
70. Wang Y., Luo C., Li J., Yin H., Li X., Zhang G. Characterization of PBDEs in soils and vegetations near an e-waste recycling site in South China. Environ. Pollut. 2011, 159:2443-2448.
71. Walker G.C. Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol. Rev. 1984, 48:60-93.
72. Environmental Health Criteria 162, Brominated Diphenyl Ethers 1994, WHO, International Program on Chemical Safety, Geneva, Switzerland.
73. Yogui G.T., Santos M.C., Bertozzi C.P., Sericano J.L., Montone R.C. PBDEs in the blubber of marine mammals from coastal areas of São Paulo, Brazil, southwestern Atlantic. Mar. Pollut. Bull. 2011, 62:2666-2670.
74. Zhu W., Liu L., Zou P., Xiao L. Effect of decabromodiphenyl ether (BDE 209) on soil microbial activity and bacterial community composition. World. J. Microbiol. Biotechnol 2010, 26:1891-1899.
75. Zhou J., Jiang W., Ding J., Zhang X., Gao Effect of Tween 80 and β-cyclodextrin on degradation of decabromodiphenyl ether (BDE-209) by white rot fungi. Chemosphere 2007, 70:172-177.
76. Zhang S., Xia X., Xia N., Wu S., Gao F., Zhou W. Identification and biodegradation efficiency of a newly isolated 2,2',4,4'-tetrabromodiphenyl ether (BDE-47) aerobic degrading bacterial strain. Int. Biodeterior. Biodegrad. 2013, 76:24-31.