Pollution and biodegradation of hexabromocyclododecanes: A review

Abstract

• Bioremediation is the most cost-effective approach for degradation of HBCDs.

• Bacteria or bacterial consortia are used in the cases of bio-augmentation.

• Microbes combined with phytoremediation increase the remediation efficiency.

Hexabromocyclododecanes (HBCDs) are the most common brominated flame-retardants after polybrominated diphenyl ethers. HBCDs can induce cancer by causing inappropriate antidiuretic hormone syndrome. Environmental contamination with HBCDs has been detected globally, with concentrations ranging from ng to mg. Methods to degrade HBCDs include physicochemical methods, bioremediation, and phytoremediation. The photodegradation of HBCDs using simulated sunlight or ultraviolet lamps, or chemical catalysts are inefficient and expensive, as is physicochemical degradation. Consequently, bioremediation is considered as the most cost-effective and clean approach. To date, five bacterial strains capable of degrading HBCDs have been isolated and identified: Pseudomonas sp. HB01, Bacillus sp. HBCD-sjtu, Achromobacter sp. HBCD-1, Achromobacter sp. HBCD-2, and Pseudomonas aeruginosa HS9. The molecular mechanisms of biodegradation of HBCDs are discussed in this review. New microbial resources should be explored to increase the resource library in order to identify more HBCD-degrading microbes and functional genes. Synthetic biology methods may be exploited to accelerate the biodegradation capability of existing bacteria, including modification of the degrading strains or functional enzymes, and artificial construction of the degradation microflora. The most potentially useful method is combining micro-degradation with physicochemical methods and phytoremediation. For example, exogenous microorganisms might be used to stimulate the adsorption capability of plants for HBCDs, or to utilize an interaction between exogenous microorganisms and rhizosphere microorganisms to form a new rhizosphere microbial community to enhance the biodegradation and absorption of HBCDs.

Graphical abstract

Keywords

Hexabromocyclododecane / Biodegradation / Bioremediation / Phytoremediation / Bacterium

References

[1] Abdallah M A, Harrad S (2011). Tetrabromobisphenol-A, hexabromocyclododecane and its degradation products in UK human milk: Relationship to external exposure. Environment International, 37(2): 443–448

[2] Arita S, Yamaguchi K, Motokucho S, Nakatani H (2017). Selective decomposition of hexabromocyclododecane in polystyrene with a photo and thermal hybrid treatment system. Polymer Degradation & Stability, 143: 130–135

[3] Batty L C, Anslow M (2008). Effect of a polycyclic aromatic hydrocarbon on the phytoremediation of zinc by two plant species (Brassica juncea and Festuca arundinacea). International Journal of Phytoremediation, 10(3): 236–249

[4] Brett H R, Marc L, Daniel P, Robert R B, John H K, Paul E H (1998). The potential of Thlaspi caerulescens for phytoremediation of contaminated soils. Plant and Soil, 203(1): 47–56

[5] Brooks R R (1977). Copper and cobalt uptake by Haumaniastrum species. Plant and Soil, 48(2): 541–544

[6] Carignan C C, Abdallah M A, Wu N, Heiger-Bernays W, McClean M D, Harrad S, Webster T F (2012). Predictors of tetrabromobisphenol-A (TBBP-A) and hexabromocyclododecanes (HBCD) in milk from Boston mothers. Environmental Science & Technology, 46(21): 12146–12153

[7] Chen J, Wang C, Pan Y, Farzana S S, Tam N F (2018). Biochar accelerates microbial reductive debromination of 2,2′4,4′-tetrabromodiphenyl ether (BDE-47) in anaerobic mangrove sediments. Journal of Hazardous Materials, 341: 177–186

[8] Chi X, Zhang Y, Wang D, Wang F, Liang W (2018). The greater roles of indigenous microorganisms in removing nitrobenzene from sediment compared with the exogenous Phragmites australis and strain JS45. Frontiers of Environmental Science & Engineering, 12(1): 11

[9] Davis J W, Gonsior S, Marty G, Ariano J (2005). The transformation of hexabromocyclododecane in aerobic and anaerobic soils and aquatic sediments. Water Research, 39(6): 1075–1084

[10] Davis J W, Gonsior S J, Markham D A, Friederich U, Hunziker R W, Ariano J M (2006). Biodegradation and product identification of [¹⁴C]hexabromocyclododecane in wastewater sludge and freshwater aquatic sediment. Environmental Science & Technology, 40(17): 5395–5401 doi:10.1021/es060009m

[11] Drage D, Mueller J F, Birch G, Eaglesham G, Hearn L K, Harrad S (2015). Historical trends of PBDEs and HBCDs in sediment cores from Sydney estuary, Australia. Science of the Total Environment, 512–513: 177–184

[12] Ema M, Fujii S, Hirata-Koizumi M, Matsumoto M (2008). Two-generation reproductive toxicity study of the flame retardant hexabromocyclododecane in rats. Reproductive Toxicology (Elmsford, N.Y.), 25(3): 335–351

[13] Fennell D E, Nijenhuis I, Wilson S F, Zinder S H, Häggblom M M (2004). Dehalococcoides ethenogenes strain 195 reductively dechlorinates diverse chlorinated aromatic pollutants. Environmental Science & Technology, 38(7): 2075–2081

[14] Fery Y, Buschauer I, Salzig C, Lang P, Schrenk D (2009). Technical pentabromodiphenyl ether and hexabromocyclododecane as activators of the pregnane-X-receptor (PXR). Toxicology, 264(1–2): 45–51

[15] Fonseca V M, Jr V J F, Araujo A S, Carvalho L H, Souza A G (2005). Effect of halogenated flame-retardant additives in the pyrolysis and thermal degradation of polyester/sisal composites. Journal of Thermal Analysis and Calorimetry, 79(2): 429–433

[16] Garg N, Bala K, Lal R (2012). Sphingobium lucknowense sp. nov., a hexachlorocyclohexane (HCH)-degrading bacterium isolated from HCH-contaminated soil. International Journal of Systematic and Evolutionary Microbiology, 62(3): 618–623

[17] Glick B R (2003). Phytoremediation: Synergistic use of plants and bacteria to clean up the environment. Biotechnology Advances, 21(5): 383–393

[18] Ha N T H, Sakakibara, M, Sano S (2010). Phytoremediation of Sb, As, Cu, and Zn from contaminated water by the aquatic macrophyte eleocharis acicularis. Clean- Soil Air Water, 37(9): 720–725

[19] He J, Ritalahti K M, Yang K L, Koenigsberg S S, Löffler F E (2003). Detoxification of vinyl chloride to ethene coupled to growth of an anaerobic bacterium. Nature, 424(6944): 62–65

[20] Heeb N V, Wyss S A, Geueke B, Fleischmann T, Kohler H E, Lienemann P (2014). LinA2, a HCH-converting bacterial enzyme that dehydrohalogenates HBCDs. Chemosphere, 107: 194–202

[21] Ho K F, Ho S S H, Lee S C, Cheng J, Watson J, Louie P K K, Tian L (2009). Emissions of gas- and particle-phase polycyclic aromatic hydrocarbons (PAHs) in the Shing Mun Tunnel, Hong Kong. Atmospheric Environment, 43(40): 6343–6351

[22] Huang L, Wang W, Shah S B, Hu H, Xu P, Tang H (2019). The HBCDs biodegradation using a Pseudomonas strain and its application in soil phytoremediation. Journal of Hazardous Materials, 380: 120833

[23] Kim G B, Stapleton H M (2010). PBDEs, methoxylated PBDEs and HBCDs in Japanese common squid (Todarodes pacificus) from Korean offshore waters. Marine Pollution Bulletin, 60(6): 935–940PMID:20394952

[24] Košnář Z, Částková T, Wiesnerová L, Praus L, Jablonský I, Koudela M, Tlustoš P (2019). Comparing the removal of polycyclic aromatic hydrocarbons in soil after different bioremediation approaches in relationto the extracellular enzyme activities. Journal of Environmental Sciences-China, 76(2): 249–258

[25] Lee L K, Ding C, Yang K L, He J (2011). Complete debromination of tetra- and penta-brominated diphenyl ethers by a coculture consisting of dehalococcoides and desulfovibrio species. Environmental Science & Technology, 45(19): 8475–8482

[26] Li L, Weber R, Liu J, Hu J (2016). Long-term emissions of hexabromocyclododecane as a chemical of concern in products in China. Environment International, 91: 291–300

[27] Li Y, Wang L, Zhu X, Gao Y, Chen J (2017). Determination of hexabromocyclododecanes in ambient air by high performance liquid chromatography- electrospray ionization-mass spectrometry. Se Pu, 35(10): 1080–1085 (in Chinese)

[28] Liu Q, Li M, Liu R, Zhang Q, Wu D, Zhu D N, Shen X H, Feng C P, Zhang F W, Liu X (2019). Removal of trimethoprim and sulfamethoxazole in artificial composite soil treatment systems and diversity of microbial communities. Frontiers of Environmental Science & Engineering, 13(2): 28 doi.org/10.1007/s11783-019-1112-9

[29] Liu Q, Li M, Liu X, Zhang Q, Liu R, Wang Z, Shi X, Quan J, Shen X, Zhang F (2018). Removal of sulfamethoxazole and trimethoprim from reclaimed water and the biodegradation mechanism. Frontiers of Environmental Science & Engineering, 12(6): 6 doi.org/10.1007/s11783-018-1048-5

[30] Liu W W, Yin R, Lin X G, Zhang J, Chen X M, Li X Z, Yang T (2010). Interaction of biosurfactant-microorganism to enhance phytoremediation of aged polycyclic aromatic hydrocarbons (PAHS) contaminated soils with alfalfa (Medicago sativa L.). Environmental Science, 31(4): 1079–1084 (in Chinese)

[31] Lu J F, He M J, Yang Z H, Wei S Q (2018). Occurrence of tetrabromobisphenol a (TBBPA) and hexabromocyclododecane (HBCD) in soil and road dust in Chongqing, western China, with emphasis on diastereoisomer profiles, particle size distribution, and human exposure. Environmental Pollution, 242(A): 219–228

[32] Luijten M L G C, de Weert J, Smidt H, Boschker H T S, de Vos W M, Schraa G, Stams A J M (2003). Description of Sulfurospirillum halorespirans sp. nov., an anaerobic, tetrachloroethene-respiring bacterium, and transfer of Dehalospirillum multivorans to the genus Sulfurospirillum as Sulfurospirillum multivorans comb. nov. International Journal of Systematic and Evolutionary Microbiology, 53(3): 787–793

[33] Maymó-Gatell X, Chien Y, Gossett J M, Zinder S H (1997). Isolation of a bacterium that reductively dechlorinates tetrachloroethene to ethene. Science, 276(5318): 1568–1571

[34] Minh N H, Isobe T, Ueno D, Matsumoto K, Mine M, Kajiwara N, Takahashi S, Tanabe S (2007). Spatial distribution and vertical profile of polybrominated diphenyl ethers and hexabromocyclododecanes in sediment core from Tokyo Bay, Japan. Environmental Pollution, 148(2): 409–417

[35] Munschy C, Marchand P, Venisseau A, Veyrand B, Zendong Z (2013). Levels and trends of the emerging contaminants HBCDs (hexabromocyclododecanes) and PFCs (perfluorinated compounds) in marine shellfish along French coasts. Chemosphere, 91(2): 233–240

[36] Muthu I G S, Nirkayani B, Kavithakani A, Padmanaban V C (2019). Statistical modeling of radiolytic (60Coγ) degradation of ofloxacin, antibiotic: Synergetic effect, kinetic studies & assessment of its degraded metabolites. Frontiers of Environmental Science & Engineering, 13(3): 42

[37] Ni H G, Zeng H (2013). HBCD and TBBPA in particulate phase of indoor air in Shenzhen, China. Science of the Total Environment, 458– 460: 15–19

[38] Palace V P, Pleskach K, Halldorson T, Danell R, Wautier K, Evans B, Alaee M, Marvin C, Tomy G T (2008). Biotransformation enzymes and thyroid axis disruption in juvenile rainbow trout (Oncorhynchus mykiss) exposed to hexabromocyclododecane diastereoisomers. Environmental Science & Technology, 42(6): 1967–1972

[39] Peng X, Huang X, Jing F, Zhang Z, Wei D, Jia X (2015). Study of novel pure culture HBCD-1, effectively degrading Hexabromocyclododecane, isolated from an anaerobic reactor. Bioresource Technology, 185: 218–224

[40] Peng X, Wei D, Huang Q, Jia X (2018). Debromination of hexabromocyclododecane by anaerobic consortium and characterization of functional bacteria. Frontiers in Microbiology, 9: 1515

[41] POPRC (2011). Report of the persisitent organic pollutants review committee on the work of its seventh meeting: Risk management evaluation on hexabromocyclododecane. Geneva: POPRC

[42] Scholz-Muramatsu H, Neumann A, Messmer M, Moore E, Diekert G (1995). Isolation and characterization of Dehalospirillum multivorans gen. nov., sp. nov., a tetrachloroethene-utilizing, strictly anaerobic bacterium. Archives of Microbiology, 163(1): 4856

[43] Shah S B, Ali F, Huang L, Wang W, Xu P, Tang H (2018). Complete genome sequence of Bacillus sp. HBCD-sjtu, an efficient HBCD-degrading bacterium. 3Biotech, 8(7): 291

[44] Shah S B, Hu H Y, Wang W W, Liu Y F, Ali F, Xu P, Tang H Z (2019a). Evaluation of plant growth promoting (PGP) activity of strain HBCD-sjtu. Journal of Biological Regulators and Homeostatic Agents, 33: 129–134

[45] Shah S B, Kaushik A C, Ali F, Huang L, Lu X, Sartaj L, Xu P, Tang H (2019b). Computational and in vitro analysis of an HBCD degrading gene DehHZ1 from strain HBCD-sjtu. Journal of Biological Regulators and Homeostatic Agents, 33(1): 157–162

[46] Stiborova H, Vrkoslavova J, Pulkrabova J, Poustka J, Hajslova J, Demnerova K (2015). Dynamics of brominated flame retardants removal in contaminated wastewater sewage sludge under anaerobic conditions. Science of the Total Environment, 533: 439–445

[47] Su J, Lu Y, Liu Z, Gao S, Zeng X, Yu Z, Sheng G, Fu J M (2015). Distribution of polybrominated diphenyl ethers and HBCD in sediments of the Hunhe River in Northeast China. Environmental Science and Pollution Research International, 22(21): 16781–16790

[48] Sun R, Luo X, Zheng X, Cao K, Peng P, Li Q X, Mai B (2018). Hexabromocyclododecanes (HBCDs) in fish: Evidence of recent HBCD input into the coastal environment. Marine Pollution Bulletin, 126: 357–362

[49] Szabo D T, Diliberto J J, Hakk H, Huwe J K, Birnbaum L S (2011). Toxicokinetics of the flame retardant hexabromocyclododecane alpha: effect of dose, timing, route, repeated exposure, and metabolism. Toxicological Sciences, 121(2): 234–244

[50] Van der Ven L T, Verhoef A, van de Kuil T, Slob W, Leonards P E, Visser T J, Hamers T, Herlin M, Håkansson H, Olausson H, Piersma A H, Vos J G (2006). A 28-day oral dose toxicity study enhanced to detect endocrine effects of hexabromocyclododecane in Wistar rats. Toxicological Sciences, 94(2): 281–292

[51] Wu T, Huang H, Zhang S (2016). Accumulation and phytotoxicity of technical hexabromocyclododecane in maize. Journal of Environmental Sciences-China, 42(4): 97–104

[52] Wu T, Wang S, Huang H, Zhang S (2012). Diastereomer-specific uptake, translocation, and toxicity of hexabromocyclododecane diastereoisomers to maize. Journal of Agricultural and Food Chemistry, 60(34): 8528–8534

[53] Xia J, Wang H, Stanford R L, Pan G, Yu S L (2018). Hydrologic and water quality performance of a laboratory scale bioretention unit. Frontiers of Environmental Science & Engineering, 12(1): 14

[54] Xian Q, Ramu K, Isobe T, Sudaryanto A, Liu X, Gao Z, Takahashi S, Yu H, Tanabe S (2008). Levels and body distribution of polybrominated diphenyl ethers (PBDEs) and hexabromocyclododecanes (HBCDs) in freshwater fishes from the Yangtze River, China. Chemosphere, 71(2): 268–276

[55] Yamada T, Takahama Y, Yamada Y (2009). Isolation of Pseudomonas sp. strain HB01 which degrades the persistent brominated flame retardant g-hexabromocyclododecane. Nippon Nogeikagaku Kaishi, 73(7): 1674–1678

[56] Yi S, Liu J G, Jin J, Zhu J (2016). Assessment of the occupational and environmental risks of hexabromocyclododecane (HBCD) in China. Chemosphere, 150: 431–437

[57] Zhang H, Kuo Y Y, Gerecke A C, Wang J (2012a). Co-release of hexabromocyclododecane (HBCD) and Nano- and microparticles from thermal cutting of polystyrene foams. Environmental Science & Technology, 46(20): 10990–10996

[58] Zhang K, Huang J, Wang H, Liu K, Yu G, Deng S, Wang B (2014). Mechanochemical degradation of hexabromocyclododecane and approaches for the remediation of its contaminated soil. Chemosphere, 116: 40–45

[59] Zhang X, Yang H, Cui Z (2017). Alleviating effect and mechanism of flavonols in Arabidopsis resistance under Pb-HBCD stress. ACS Sustainable Chemistry & Engineering, 5(11): 11034–11041

[60] Zhang Y, Ruan Y, Sun H, Zhao L, Gan Z (2013). Hexabromocyclododecanes in surface sediments and a sediment core from Rivers and Harbor in the northern Chinese city of Tianjin. Chemosphere, 90(5): 1610–1616

[61] Zhang Y, Wang H, Yu Z, Geng X, Chen C, Li D, Zhu X, Zhen H, Huang W, Fennell D E, Young L Y, Peng P (2018). Diastereoisomer-specific biotransformation of hexabromocyclododecanes by a mixed culture containing Dehalococcoides mccartyi strain 195. Frontiers in Microbiology, 9: 1713

[62] Zhang Z, Rengel Z, Chang H, Meney K, Pantelic L, Tomanovc R (2012b). Phytoremediation potential of Juncus subsecundus in soils contaminated with cadmium and polynuclear aromatic hydrocarbons (PAHs). Geoderma, 175–176: 1–8

[63] Zheng X, Qiao L, Sun R, Luo X, Zheng J, Xie Q, Sun Y, Mai B (2017). Alteration of diastereoisomeric and enantiomeric profiles of hexabromocyclododecanes (HBCDs) in adult chicken tissues, eggs, and hatchling chickens. Environmental Science & Technology, 51(10): 5492–5499

[64] Zhou D, Wu Y, Feng X, Chen Y, Wang Z, Tao T, Wei D (2014). Photodegradation of hexabromocyclododecane (HBCD) by Fe(III) complexes/H₂O₂ under simulated sunlight. Environmental Science and Pollution Research International, 21(9): 6228–6233

RIGHTS & PERMISSIONS

Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature