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Diversity of organohalide respiring bacteria and reductive dehalogenases that detoxify polybrominated diphenyl ethers in E-waste recycling sites

Abstract

Widespread polybrominated diphenyl ethers (PBDEs) contamination poses risks to human health and ecosystems. Bioremediation is widely considered to be a less ecologically disruptive strategy for remediation of organohalide contamination, but bioremediation of PBDE-contaminated sites is limited by a lack of knowledge about PBDE-dehalogenating microbial populations. Here we report anaerobic PBDE debromination in microcosms established from geographically distinct e-waste recycling sites. Complete debromination of a penta-BDE mixture to diphenyl ether was detected in 16 of 24 investigated microcosms; further enrichment of these 16 microcosms implicated microbial populations belonging to the bacterial genera Dehalococcoides, Dehalogenimonas, and Dehalobacter in PBDE debromination. Debrominating microcosms tended to contain either both Dehalogenimonas and Dehalobacter or Dehalococcoides alone. Separately, complete debromination of a penta-BDE mixture was also observed by axenic cultures of Dehalococcoides mccartyi strains CG1, CG4, and 11a5, suggesting that this phenotype may be fairly common amongst Dehalococcoides. PBDE debromination in these isolates was mediated by four reductive dehalogenases not previously known to debrominate PBDEs. Debromination of an octa-BDE mixture was less prevalent and less complete in microcosms. The PBDE reductive dehalogenase homologous genes in Dehalococcoides genomes represent plausible molecular markers to predict PBDE debromination in microbial communities via their prevalence and transcriptions analysis.

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Fig. 1: Debromination of PBDEs in microcosms established from soil and sediments collected from 24 geographically distinct e-waste contaminated sites.
Fig. 2: Correlations between the abundance of Dehalococcoides, Dehalogenimonas and Dehalobacter and removal of bromine from a penta-BDE mixture in enrichment cultures.
Fig. 3: Debromination of a penta- and an octa- BDE mixture by Dehalococcoides isolates.
Fig. 4: Debromination pathways of a penta-BDE mixture and hepta-BDE 183 by Dehalococcoides isolates.
Fig. 5: Identification of PBDEs reductive dehalogenases (RDases).
Fig. 6: Prevelance and activity of identified PBDE reductive dehalogenase homologous genes (rdh).

Data availability

All data generated or analysed during this study are included in this published article and its supplementary information files.

References

  1. Statista (2020). ‘Consumer Electronics’: Statista, Hamburg, Germany.

  2. Bacher J, Dams Y, Duhoux T, Deng Y, Teittinen T, Mortensen LF. Electronic products and obsolescence in a circular economy. European Topic Centre Waste and Materials in a Green Economy: Belgiu; 2020.

  3. Forti V, Bald CP, Kuehr R, Bel G. The Global E-waste Monitor 2020: Quantities, flows and the circular economy potential. Bonn, Geneva and Rotterdam: United Nations University/United Nations Institute for Training and Research, International Telecommunication Union, and International Solid Waste Association; 2020.

    Google Scholar 

  4. McGrath TJ, Ball AS, Clarke BO. Critical review of soil contamination by polybrominated diphenyl ethers (PBDEs) and novel brominated flame retardants (NBFRs); concentrations, sources and congener profiles. Environ Pollut. 2017;230:741–57.

    CAS  Article  Google Scholar 

  5. Lu Q, Liang Y, Fang W, Guan KL, Huang C, Qi X, et al. Spatial distribution, bioconversion and ecological risk of PCBs and PBDEs in the surface sediment of contaminated urban rivers: a nationwide study in China. Environ Sci Technol. 2021;55:9579–90.

    CAS  Article  Google Scholar 

  6. Li WL, Ma WL, Jia HL, Hong WJ, Moon HB, Nakata H, et al. Polybrominated diphenyl ethers (PBDEs) in surface soils across five Asian countries: levels, spatial distribution, and source contribution. Environ Sci Technol. 2016;50:12779–88.

    CAS  Article  Google Scholar 

  7. Zhao S, Rogers MJ, Ding C, He J. Reductive debromination of polybrominated diphenyl ethers - microbes, processes and dehalogenases. Front Microbiol. 2018;9:1292.

    Article  Google Scholar 

  8. Ding C, Rogers MJ, Yang KL, He J. Loss of the ssrA genome island led to partial debromination in the PBDE respiring Dehalococcoides mccartyi strain GY50. Environ Microbiol. 2017;19:2906–15.

    CAS  Article  Google Scholar 

  9. Zhao S, Rogers MJ, Cao L, Ding C, He J. Identification of reductive dehalogenases that mediate complete debromination of penta- and tetrabrominated diphenyl ethers in Dehalococcoides spp. Appl Environ Microbiol. 2021;87:e0060221.

    Article  Google Scholar 

  10. Ding C, He J. Molecular techniques in the biotechnological fight against halogenated compounds in anoxic environments. Micro Biotechnol. 2012;5:347–67.

    Article  Google Scholar 

  11. Lee PK, Johnson DR, Holmes VF, He J, Alvarez-Cohen L. Reductive dehalogenase gene expression as a biomarker for physiological activity of Dehalococcoides spp. Appl Environ Microbiol. 2006;72:6161–8.

    CAS  Article  Google Scholar 

  12. Shrivastava A, Gupta V. Methods for the determination of limit of detection and limit of quantitation of the analytical methods. Chron Young- Scientists. 2011;2:21.

    Article  Google Scholar 

  13. Wang S, Chng KR, Wilm A, Zhao S, Yang K-L, Nagarajan N, et al. Genomic characterization of three unique Dehalococcoides that respire on persistent polychlorinated biphenyls. Proc Natl Acad Sci USA. 2014;111:12103–8.

    CAS  Article  Google Scholar 

  14. He J, Holmes VF, Lee PK, Alvarez-Cohen L. Influence of vitamin B12 and cocultures on the growth of Dehalococcoides isolates in defined medium. Appl Environ Microbiol. 2007;73:2847–53.

    CAS  Article  Google Scholar 

  15. Ding C, Rogers MJ, He J. Dehalococcoides mccartyi strain GEO12 has a natural tolerance to chloroform inhibition. Environ Sci Technol. 2020;54:8750–9.

    CAS  Article  Google Scholar 

  16. Lee PK, Cheng D, West KA, Alvarez-Cohen L, He J. Isolation of two new Dehalococcoides mccartyi strains with dissimilar dechlorination functions and their characterization by comparative genomics via microarray analysis. Environ Microbiol. 2013;15:2293–305.

    CAS  Article  Google Scholar 

  17. Ding C, Chow WL, He J. Isolation of Acetobacterium sp. strain AG, which reductively debrominates octa- and pentabrominated diphenyl ether technical mixtures. Appl Environ Microbiol. 2013;79:1110–7.

    CAS  Article  Google Scholar 

  18. Schiffmann CL, Jehmlich N, Otto W, Hansen R, Nielsen PH, Adrian L, et al. Proteome profile and proteogenomics of the organohalide-respiring bacterium Dehalococcoides mccartyi strain CBDB1 grown on hexachlorobenzene as electron acceptor. J Proteom. 2014;98:59–64.

    CAS  Article  Google Scholar 

  19. Zhao S, Ding C, He J. Genomic characterization of Dehalococcoides mccartyi strain 11a5 reveals a circular extrachromosomal genetic element and a new tetrachloroethene reductive dehalogenase gene. FEMS Microbiol Ecol. 2017;93:fiw235.

    Google Scholar 

  20. Perez-Riverol Y, Csordas A, Bai J, Bernal-Llinares M, Hewapathirana S, Kundu DJ, et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 2019;47:D442–D450.

    CAS  Article  Google Scholar 

  21. He J, Robrock KR, Alvarez-Cohen L. Microbial reductive debromination of polybrominated diphenyl ethers (PBDEs). Environ Sci Technol. 2006;40:4429–34.

    CAS  Article  Google Scholar 

  22. Robrock KR, Korytar P, Alvarez-Cohen L. Pathways for the anaerobic microbial debromination of polybrominated diphenyl ethers. Environ Sci Technol. 2008;42:2845–52.

    CAS  Article  Google Scholar 

  23. Yang Y, Higgins SA, Yan J, Simsir B, Chourey K, Iyer R, et al. Grape pomace compost harbors organohalide-respiring Dehalogenimonas species with novel reductive dehalogenase genes. ISME J. 2017;11:2767–80.

    CAS  Article  Google Scholar 

  24. Qiao W, Luo F, Lomheim L, Mack EE, Ye S, Wu J, et al. A Dehalogenimonas population respires 1,2,4-trichlorobenzene and dichlorobenzenes. Environ Sci Technol. 2018;52:13391–8.

    CAS  Article  Google Scholar 

  25. Moe WM, Yan J, Nobre MF, da Costa MS, Rainey FA. Dehalogenimonas lykanthroporepellens gen. nov., sp. nov., a reductively dehalogenating bacterium isolated from chlorinated solvent-contaminated groundwater. Int J Syst Evol Microbiol. 2009;59:2692–7.

    CAS  Article  Google Scholar 

  26. Key TA, Bowman KS, Lee I, Chun J, Albuquerque L, da Costa MS, et al. Dehalogenimonas formicexedens sp. nov., a chlorinated alkane-respiring bacterium isolated from contaminated groundwater. Int J Syst Evol Microbiol. 2017;67:1366–73.

    CAS  Article  Google Scholar 

  27. Darnerud PO, Eriksen GS, Johannesson T, Larsen PB, Viluksela M. Polybrominated diphenyl ethers: occurrence, dietary exposure, and toxicology. Environ Health Perspect. 2001;109:49–68.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Xu G, Zhao X, Zhao S, Chen C, Rogers MJ, Ramaswamy R, et al. Insights into the occurrence, fate, and impacts of halogenated flame retardants in municipal wastewater treatment plants. Environ Sci Technol. 2021;55:4205–26.

    CAS  Article  Google Scholar 

  29. Molenda O, Puentes Jacome LA, Cao X, Nesbo CL, Tang S, Morson N, et al. Insights into origins and function of the unexplored majority of the reductive dehalogenase gene family as a result of genome assembly and ortholog group classification. Environ Sci Process Impacts. 2020;22:663–78.

    CAS  Article  Google Scholar 

  30. Qiu L, Fang W, He H, Liang Z, Zhan Y, Lu Q, et al. Organohalide-respiring bacteria in polluted urban rivers employ novel bifunctional reductive dehalogenases to dechlorinate polychlorinated biphenyls and tetrachloroethene. Environ Sci Technol. 2020;54:8791–800.

    CAS  Article  Google Scholar 

  31. Adrian L, Rahnenfuhrer J, Gobom J, Holscher T. Identification of a chlorobenzene reductive dehalogenase in Dehalococcoides sp. strain CBDB1. Appl Environ Microbiol. 2007;73:7717–24.

    CAS  Article  Google Scholar 

  32. Heavner GLW, Mansfeldt CB, Wilkins MJ, Nicora CD, Debs GE, Edwards EA, et al. Detection of organohalide-respiring enzyme biomarkers at a bioaugmented TCE-contaminated field site. Front Microbiol. 2019;10:1433.

    Article  Google Scholar 

  33. Padilla-Crespo E, Yan J, Swift C, Wagner DD, Chourey K, Hettich RL, et al. Identification and environmental distribution of dcpA, which encodes the reductive dehalogenase catalyzing the dichloroelimination of 1,2-dichloropropane to propene in organohalide-respiring chloroflexi. Appl Environ Microbiol. 2014;80:808–18.

    Article  Google Scholar 

  34. Yang C, Kublik A, Weidauer C, Seiwert B, Adrian L. Reductive dehalogenation of oligocyclic phenolic bromoaromatics by Dehalococcoides mccartyi strain CBDB1. Environ Sci Technol. 2015;49:8497–505.

    CAS  Article  Google Scholar 

  35. Morris RM, Fung JM, Rahm BG, Zhang S, Freedman DL, Zinder SH, et al. Comparative proteomics of Dehalococcoides spp. reveals strain-specific peptides associated with activity. Appl Environ Microbiol. 2007;73:320–6.

    CAS  Article  Google Scholar 

  36. Ramaswamy R, Zhao S, Bae S, He J. Debromination of TetraBromoBisphenol-A (TBBPA) depicting the metabolic versatility of Dehalococcoides. J Hazard Mater. 2021;419:126408.

    CAS  Article  Google Scholar 

  37. Chow WL, Cheng D, Wang S, He J. Identification and transcriptional analysis of trans-DCE-producing reductive dehalogenases in Dehalococcoides species. ISME J. 2010;4:1020–30.

    Article  Google Scholar 

  38. Muller JA, Rosner BM, Von Abendroth G, Meshulam-Simon G, McCarty PL, Spormann AM. Molecular identification of the catabolic vinyl chloride reductase from Dehalococcoides sp. strain VS and its environmental distribution. Appl Environ Microbiol. 2004;70:4880–8.

    Article  Google Scholar 

  39. Krajmalnik-Brown R, Holscher T, Thomson IN, Saunders FM, Ritalahti KM, Löffler FE. Genetic identification of a putative vinyl chloride reductase in Dehalococcoides sp. strain BAV1. Appl Environ Microbiol. 2004;70:6347–51.

    CAS  Article  Google Scholar 

  40. Fung JM, Morris RM, Adrian L, Zinder SH. Expression of reductive dehalogenase genes in Dehalococcoides ethenogenes strain 195 growing on tetrachloroethene, trichloroethene, or 2,3-dichlorophenol. Appl Environ Microbiol. 2007;73:4439–45.

    CAS  Article  Google Scholar 

  41. Magnuson JK, Stern RV, Gossett JM, Zinder SH, Burris DR. Reductive dechlorination of tetrachloroethene to ethene by a two-component enzyme pathway. Appl Environ Microbiol. 1998;64:1270–5.

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the Ng Teng Fong Charitable Foundation (NTFCF) fund (No.: R-302-000-198-720) and the Ministry of Education, Singapore under Academic Research Fund Tier 2 project MOE-000033-01 and Tier 1 project R302000239114.We would also like to acknowledge the help kindly provided by Prof. Lorenz Adrian from Helmholtz-Centre for Environmental Research for proteomics analysis.

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SZ and JH designed the study. SZ, DC, GX, and RR performed the experiments. SZ analyzed the data and wrote the manuscript. SZ, MR and JH contributed to the revision and finalization of the manuscript.

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Correspondence to Jianzhong He.

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Zhao, S., Ding, C., Xu, G. et al. Diversity of organohalide respiring bacteria and reductive dehalogenases that detoxify polybrominated diphenyl ethers in E-waste recycling sites. ISME J 16, 2123–2131 (2022). https://doi.org/10.1038/s41396-022-01257-0

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