Advertisement

Environmental Science and Pollution Research

, Volume 26, Issue 23, pp 23832–23841 | Cite as

Aerobic cometabolism of tetrabromobisphenol A by marine bacterial consortia

  • Chen Gu
  • Jing WangEmail author
  • Zelong Zhao
  • Ying Han
  • Miaomiao Du
  • Shuaijun Zan
  • Fenbo Wang
Research Article
  • 212 Downloads

Abstract

The coastal environments worldwide are subjected to increasing TBBPA contamination, but current knowledge on aerobic biodegradability of this compound by marine microbes is lacking. The aerobic removal of TBBPA using marine consortia under eight different cometabolic conditions was investigated here. Results showed that the composition and diversity of the TBBPA-degrading consortia had diverged after 120-day incubation. Pseudoalteromonas, Alteromonas, Glaciecola, Thalassomonas, and Limnobacter were the dominant genera in enrichment cultures. Furthermore, a combination of beef extract- and peptone-enriched marine consortia exhibited higher TBBPA removal efficiency (approximately 60%) than the other substrate amendments. Additionally, Alteromonas macleodii strain GCW was isolated from a culture of TBBPA-degrading consortium. This strain exhibited about 90% of degradation efficiency toward TBBPA (10 mg L−1) after 10 days of incubation under aerobic cometabolic conditions. The intermediates in the degradation of TBBPA by A. macleodii strain GCW were analyzed and the degradation pathways were proposed, involving β-scission, debromination, and nitration routes.

Keywords

Brominated flame retardant Coastal marine sediments Aerobic removal Cometabolism Microbial community Alteromonas macleodii 

Notes

Funding information

This research was supported by the National Natural Science Foundation of China (No. 21876018).

Supplementary material

11356_2019_5660_MOESM1_ESM.docx (263 kb)
ESM 1 (DOCX 195 kb)

References

  1. An T, Zu L, Li G, Wan S, Mai B, Wong PK (2011) One-step process for debromination and aerobic mineralization of tetrabromobisphenol-A by a novel Ochrobactrum sp. T isolated from an e-waste recycling site. Bioresour Technol 102:9148–9154CrossRefGoogle Scholar
  2. Aznar-Alemany Ò, Trabalón L, Jacobs S, Barbosa VL, Tejedor MF, Granby K, Kwadijk C, Cunha SC, Ferrari F, Vandermeersch G, Sioen I, Verbeke W, Vilavert L, Domingo JL, Eljarrat E, Barceló D (2017) Occurrence of halogenated flame retardants in commercial seafood species available in European markets. Food Chem Toxicol 104:35–47CrossRefGoogle Scholar
  3. Bao Y, Niu J (2015) Photochemical transformation of tetrabromobisphenol A under simulated sunlight irradiation: kinetics, mechanism and influencing factors. Chemosphere 134:550–556CrossRefGoogle Scholar
  4. Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59CrossRefGoogle Scholar
  5. Brakstad OG, Nonstad I, Faksness LG, Brandvik PJ (2008) Responses of microbial communities in Arctic sea ice after contamination by crude petroleum oil. Microb Ecol 55:540–552CrossRefGoogle Scholar
  6. Cai WJ, Sayles FL (1996) Oxygen penetration depths and fluxes in marine sediments. Mar Chem 52:123–131CrossRefGoogle Scholar
  7. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefGoogle Scholar
  8. Chang BV, Yuan SY, Ren YL (2012) Aerobic degradation of tetrabromobisphenol-A by microbes in river sediment. Chemosphere 87:535–541CrossRefGoogle Scholar
  9. Chen Z, Yin H, Peng H, Lu G, Liu Z, Dang Z (2019) Identification of novel pathways for biotransformation of tetrabromobisphenol A by Phanerochaete chrysosporium, combined with mechanism analysis at proteome level. Sci Total Environ 659:1352–1361CrossRefGoogle Scholar
  10. Darnerud PO (2003) Toxic effects of brominated flame retardants in man and in wildlife. Environ Int 29:841–853CrossRefGoogle Scholar
  11. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072CrossRefGoogle Scholar
  12. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefGoogle Scholar
  13. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefGoogle Scholar
  14. Feng Y, Colosi LM, Gao S, Huang Q, Mao L (2013) Transformation and removal of tetrabromobisphenol A from water in the presence of natural organic matter via laccase-catalyzed reactions: reaction rates, products, and pathways. Environ Sci Technol 47:1001–1008CrossRefGoogle Scholar
  15. Feng Y, Lu K, Gao S, Mao L (2017) The fate and transformation of tetrabromobisphenol A in natural waters, mediated by oxidoreductase enzymes. Environ Sci Process Impacts 19:596–604CrossRefGoogle Scholar
  16. Fuse H, Takimura O, Murakami K, Inoue H, Yamaoka Y (2003) Degradation of chlorinated biphenyl, dibenzofuran, and dibenzo-p-dioxin by marine bacteria that degrade biphenyl, carbazole, or dibenzofuran. Biosci Biotechnol Biochem 67:1121–1125CrossRefGoogle Scholar
  17. Gao Y, Pang S, Jiang J, Ma J, Zhou Y, Li J, Wang L, Lu X, Yuan L (2016) Transformation of flame retardant tetrabromobisphenol A by aqueous chlorine and the effect of humic acid. Environ Sci Technol 50:9608–9618CrossRefGoogle Scholar
  18. George KW, Häggblom MM (2008) Microbial O-methylation of the flame retardant tetrabromobisphenol-A. Environ Sci Technol 42:5555–5561CrossRefGoogle Scholar
  19. Gong WJ, Zhu LY, Jiang TT, Cui H (2017) The occurrence and spatial-temporal distribution of tetrabromobisphenol A in the coastal intertidal zone of Qingdao in China, with a focus on toxicity assessment by biological monitoring. Chemosphere 185:462–467CrossRefGoogle Scholar
  20. Gu C, Wang J, Liu S, Liu G, Lu H, Jin R (2016) Biogenic Fenton-like reaction involvement in cometabolic degradation of tetrabromobisphenol A by Pseudomonas sp. fz. Environ Sci Technol 50:9981–9989CrossRefGoogle Scholar
  21. Gu SY, Ekpeghere KI, Kim HY, Lee IS, Kim DH, Choo G, Oh JE (2017) Brominated flame retardants in marine environment focused on aquaculture area: occurrence, source and bioaccumulation. Sci Total Environ 601-602:1182–1191CrossRefGoogle Scholar
  22. Guo Y, Zhou J, Lou X, Liu R, Xiao D, Fang C, Wang Z, Liu J (2014) Enhanced degradation of Tetrabromobisphenol A in water by a UV/base/persulfate system: kinetics and intermediates. Chem Eng J 254:538–544CrossRefGoogle Scholar
  23. Guo R, Pan L, Ji R (2017) A multi-biomarker approach in scallop Chlamys farreri to assess the impact of contaminants in Qingdao coastal area of China. Ecotoxicol Environ Saf 142:399–409CrossRefGoogle Scholar
  24. Han SK, Bilski P, Karriker B, Sik RH, Chignell CF (2008) Oxidation of flame retardant tetrabromobisphenol A by singlet oxygen. Environ Sci Technol 42:166–172CrossRefGoogle Scholar
  25. Hedlund BP, Staley JT (2006) Isolation and characterization of Pseudoalteromonas strains with divergent polycyclic aromatic hydrocarbon catabolic properties. Environ Microbiol 8:178–182CrossRefGoogle Scholar
  26. Ji Y, Kong D, Lu J, Jin H, Kang F, Yin X, Zhou Q (2016) Cobalt catalyzed peroxymonosulfate oxidation of tetrabromobisphenol A: kinetics, reaction pathways, and formation of brominated by-products. J Hazard Mater 313:229–237CrossRefGoogle Scholar
  27. Jickells TD (1998) Nutrient biogeochemistry of the coastal zone. Science 281:217–222CrossRefGoogle Scholar
  28. Jin HM, Kim JM, Lee HJ, Madsen EL, Jeon CO (2012) Alteromonas as a key agent of polycyclic aromatic hydrocarbon biodegradation in crude oil-contaminated coastal sediment. Environ Sci Technol 46:7731–7740CrossRefGoogle Scholar
  29. Kristensen E (2000) Organic matter diagenesis at the oxic/anoxic interface in coastal marine sediments, with emphasis on the role of burrowing animals. Hydrobiologia 426:1–24CrossRefGoogle Scholar
  30. Law RJ, Allchin CR, de Boer J, Covaci A, Herzke D, Lepom P, Morris S, Tronczynski J, de Wit CA (2006) Levels and trends of brominated flame retardants in the European environment. Chemosphere 64:187–208CrossRefGoogle Scholar
  31. Lawes JC, Neilan BA, Brown MV, Clark GF, Johnston EL (2016) Elevated nutrients change bacterial community composition and connectivity: high throughput sequencing of young marine biofilms. Biofouling 32:57–69CrossRefGoogle Scholar
  32. Le TT, Son MH, Nam IH, Yoon H, Kang YG, Chang YS (2017) Transformation of hexabromocyclododecane in contaminated soil in association with microbial diversity. J Hazard Mater 325:82–89CrossRefGoogle Scholar
  33. Leng Y, Bao J, Song D, Li J, Ye M, Li X (2017) Background nutrients affect the biotransformation of tetracycline by Stenotrophomonas maltophilia as revealed by genomics and proteomics. Environ Sci Technol 51:10476–10484CrossRefGoogle Scholar
  34. Li F, Wang J, Nastold P, Jiang B, Sun F, Zenker A, Kolvenbach BA, Corvini PFX (2014) Fate and metabolism of tetrabromobisphenol A in soil slurries without and with the amendment with the alkylphenol degrading bacterium Sphingomonas sp. strain TTNP3. Environ Pollut 193:181–188CrossRefGoogle Scholar
  35. Li F, Wang J, Jiang B, Yang X, Nastold P, Kolvenbach B, Wang L, Ma Y, Corvini PFX, Ji R (2015a) Fate of tetrabromobisphenol A (TBBPA) and formation of ester-and ether-linked bound residues in an oxic sandy soil. Environ Sci Technol 49:12758–12765CrossRefGoogle Scholar
  36. Li F, Jiang B, Nastold P, Kolvenbach BA, Chen J, Wang L, Guo H, Corvini PFX, Ji R (2015b) Enhanced transformation of tetrabromobisphenol A by nitrifiers in nitrifying activated sludge. Environ Sci Technol 49:4283–4292CrossRefGoogle Scholar
  37. Li G, Xiong J, Wong PK, An T (2016) Enhancing tetrabromobisphenol A biodegradation in river sediment microcosms and understanding the corresponding microbial community. Environ Pollut 208:796–802CrossRefGoogle Scholar
  38. Liang SH, Hsu DW, Lin CY, Kao CM, Huang DJ, Chien CC, Chen SC, Tsai IJ, Chen CC (2017) Enhancement of microbial 2,4,6-trinitrotoluene transformation with increased toxicity by exogenous nutrient amendment. Ecotoxicol Environ Saf 138:39–46CrossRefGoogle Scholar
  39. Liang Z, Li G, Mai B, Ma H, An T (2019) Application of a novel gene encoding bromophenol dehalogenase from Ochrobactrum sp. T in TBBPA degradation. Chemosphere 217:507–515CrossRefGoogle Scholar
  40. Lin K, Liu W, Gan J (2009) Reaction of tetrabromobisphenol A (TBBPA) with manganese dioxide: kinetics, products, and pathways. Environ Sci Technol 43:4480–4486CrossRefGoogle Scholar
  41. Liu HH, Hu YJ, Luo P, Bao LJ, Qiu JW, Leung KMY, Zeng EY (2014) Occurrence of halogenated flame retardants in sediment off an urbanized coastal zone: association with urbanization and industrialization. Environ Sci Technol 48:8465–8473CrossRefGoogle Scholar
  42. Liu A, Qu G, Yu M, Liu Y, Shi J, Jiang G (2016) Tetrabromobisphenol-A/S and nine novel analogs in biological samples from the Chinese Bohai Sea: implications for trophic transfer. Environ Sci Technol 50:4203–4211CrossRefGoogle Scholar
  43. Liu S, Wawrik B, Liu Z (2017) Different bacterial communities involved in peptide decomposition between normoxic and hypoxic coastal waters. Front Microbiol 8:353Google Scholar
  44. López-López A, Bartual SG, Stal L, Onyshchenko O, Rodríguez-Valera F (2005) Genetic analysis of housekeeping genes reveals a deep-sea ecotype of Alteromonas macleodii in the Mediterranean Sea. Environ Microbiol 7:649–659CrossRefGoogle Scholar
  45. Lu K, Huang Q, Xia T, Chang X, Wang P, Gao S, Mao L (2017) The potential ecological risk of multiwall carbon nanotubes was modified by the radicals resulted from peroxidase-mediated tetrabromobisphenol A reactions. Environ Pollut 220:264–273CrossRefGoogle Scholar
  46. Lv Y, Li L, Chen Y, Tang Z, Hu Y (2016) Effects of glucose and biphenyl on aerobic cometabolism of polybrominated diphenyl ethers by Pseudomonas putida: kinetics and degradation mechanism. Int Biodeterior Biodegrad 108:76–84CrossRefGoogle Scholar
  47. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963CrossRefGoogle Scholar
  48. Meerts IA, van Zanden JJ, Luijks EA, van Leeuwen-Bol I, Marsh G, Jakobsson E, Bergman Å, Brouwer A (2000) Potent competitive interactions of some brominated flame retardants and related compounds with human transthyretin in vitro. Toxicol Sci 56:95–104CrossRefGoogle Scholar
  49. Michaud L, Di Marco G, Bruni V, Giudice AL (2007) Biodegradative potential and characterization of psychrotolerant polychlorinated biphenyl-degrading marine bacteria isolated from a coastal station in the Terra Nova Bay (Ross Sea, Antarctica). Mar Pollut Bull 54:1754–1761CrossRefGoogle Scholar
  50. Mitulla M, Dinasquet J, Guillemette R, Simon M, Azam F, Wietz M (2016) Response of bacterial communities from California coastal waters to alginate particles and an alginolytic Alteromonas macleodii strain. Environ Microbiol 18:4369–4377CrossRefGoogle Scholar
  51. Nyholm JR, Lundberg C, Andersson PL (2010) Biodegradation kinetics of selected brominated flame retardants in aerobic and anaerobic soil. Environ Pollut 158:2235–2240CrossRefGoogle Scholar
  52. Palenik B, Ren Q, Dupont CL, Myers GS, Heidelberg JF, Badger JH, Madupu R, Nelson WC, Brinkac LM, Dodson RJ, Durkin AS, Daugherty SC, Sullivan SA, Khouri H, Mohamoud Y, Halpin R, Paulsen IT (2006) Genome sequence of Synechococcus CC9311: insights into adaptation to a coastal environment. Proc Natl Acad Sci USA 103:13555–13559CrossRefGoogle Scholar
  53. Peng FQ, Ying GG, Yang B, Liu YS, Lai HJ, Zhou GJ, Chen J, Zhao JL (2014) Biotransformation of the flame retardant tetrabromobisphenol-A (TBBPA) by freshwater microalgae. Environ Toxicol Chem 33:1705–1711CrossRefGoogle Scholar
  54. Peng X, Wang Z, Huang J, Pittendrigh BR, Liu S, Jia X, Wong PK (2017) Efficient degradation of tetrabromobisphenol A by synergistic integration of Fe/Ni bimetallic catalysis and microbial acclimation. Water Res 122:471–480CrossRefGoogle Scholar
  55. Qu R, Feng M, Wang X, Huang Q, Lu J, Wang L, Wang Z (2015) Rapid removal of tetrabromobisphenol A by ozonation in water: oxidation products, reaction pathways and toxicity assessment. PLoS One 10:e0139580CrossRefGoogle Scholar
  56. Samarakoon K, Jeon YJ (2012) Bio-functionalities of proteins derived from marine algae. A review. Food Res Int 48:948–960CrossRefGoogle Scholar
  57. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefGoogle Scholar
  58. Schumacher BA (2002) Methods for the determination of total organic carbon (TOC) in soils and sediments. Ecological Risk Assessment Support Center. United States Environmental Protection Agency, Las VegasGoogle Scholar
  59. Shi G, Yin H, Ye J, Peng H, Li J, Luo C (2013) Aerobic biotransformation of decabromodiphenyl ether (PBDE-209) by Pseudomonas aeruginosa. Chemosphere 93:1487–1493CrossRefGoogle Scholar
  60. Sparks DL (1996) Methods of Soil Analysis Part 3. Chemical methods. Soil Science Society of America, MadisonGoogle Scholar
  61. Stiborova H, Vrkoslavova J, Lovecka P, Pulkrabova J, Hradkova P, Hajslova J, Demnerova K (2015) Aerobic biodegradation of selected polybrominated diphenyl ethers (PBDEs) in wastewater sewage sludge. Chemosphere 118:315–321CrossRefGoogle Scholar
  62. Sühring R, Barber JL, Wolschke H, Kötke D, Ebinghaus R (2015) Fingerprint analysis of brominated flame retardants and Dechloranes in North Sea sediments. Environ Res 140:569–578CrossRefGoogle Scholar
  63. Tengberg A, Almroth E, Hall P (2003) Resuspension and its effects on organic carbon recycling and nutrient exchange in coastal sediments: in situ measurements using new experimental technology. J Exp Mar Biol Ecol 285-286:119–142CrossRefGoogle Scholar
  64. Vedler E, Heinaru E, Jutkina J, Viggor S, Koressaar T, Remm M, Heinaru A (2013) Limnobacter spp. as newly detected phenol-degraders among Baltic Sea surface water bacteria characterised by comparative analysis of catabolic genes. Syst Appl Microbial 36:525–532CrossRefGoogle Scholar
  65. Vila J, Grifoll M (2009) Actions of Mycobacterium sp. strain AP1 on the saturated-and aromatic-hydrocarbon fractions of fuel oil in a marine medium. Appl Environ Microbiol 75:6232–6239CrossRefGoogle Scholar
  66. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefGoogle Scholar
  67. Wang X, Hu X, Zhang H, Chang F, Luo Y (2015) Photolysis kinetics, mechanisms, and pathways of tetrabromobisphenol A in water under simulated solar light irradiation. Environ Sci Technol 49:6683–6690CrossRefGoogle Scholar
  68. Xie H, Wang H, Ji F, Liang Y, Song M, Zhang J (2018) Tetrabromobisphenol A alters soil microbial community via selective antibacterial activity. Ecotoxicol Environ Saf 164:597–603CrossRefGoogle Scholar
  69. Xu S, Wang YF, Yang LY, Ji R, Miao AJ (2017) Transformation of tetrabromobisphenol A by Rhodococcus jostii RHA1: effects of heavy metals. Chemosphere 196:206–213CrossRefGoogle Scholar
  70. Yang B, Ying GG, Chen ZF, Zhao JL, Peng FQ, Chen XW (2014) Ferrate (VI) oxidation of tetrabromobisphenol A in comparison with bisphenol A. Water Res 62:211–219CrossRefGoogle Scholar
  71. Yang CW, Chen WZ, Chang BV (2017) Biodegradation of tetrabromobisphenol-A in sludge with spent mushroom compost. Int Biodeterior Biodegrad 119:387–395CrossRefGoogle Scholar
  72. Zhong Y, Liang X, Zhong Y, Zhu J, Zhu S, Yuan P, He H, Zhang J (2012) Heterogeneous UV/Fenton degradation of TBBPA catalyzed by titanomagnetite: catalyst characterization, performance and degradation products. Water Res 46:4633–4644CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education), School of Environmental Science and TechnologyDalian University of TechnologyDalianChina

Personalised recommendations