Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Substantial defluorination of polychlorofluorocarboxylic acids triggered by anaerobic microbial hydrolytic dechlorination

Nature Water volume 1, pages 451–461 (2023)Cite this article

Subjects

Abstract

Chlorinated polyfluorocarboxylic acids (Cl-PFCAs) derived from the widely used chlorotrifluoroethylene oligomers and polymers may enter and influence the aquatic environment. Here we report the substantial defluorination of Cl-PFCAs by an anaerobic microbial community via novel pathways triggered by anaerobic microbial dechlorination. Cl-PFCAs first underwent microbial reductive, hydrolytic and eliminative dechlorination, with the hydrolytic dechlorination leading to the highest spontaneous defluorination. Hydrolytic dechlorination was favoured with increased Cl substitutions. An isolated, highly enriched, anaerobic defluorinating culture was dominated by two genomes that were most similar to those of Desulfovibrio aminophilus and Sporomusa sphaeroides, both of which exhibited defluorination activity towards chlorotrifluoroethylene tetramer acid. The results imply that anaerobic non-respiratory hydrolytic dechlorination plays a critical role in the fate of chlorinated polyfluoro chemicals in natural and engineered water environments. The greatly enhanced biodegradability by Cl substitution also sheds light on the design of cost-effective treatment biotechnologies, as well as alternative polyfluoroalkyl substances that are readily biodegradable and less toxic.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Biotransformation and defluorination pathways of CTFE oligomer carboxylic acids by the anaerobic microbial community.
Fig. 2: Biotransformation and defluorination pathways of CTFE2 by the anaerobic microbial community.
Fig. 3: Biotransformation and defluorination of CTFE3 by the anaerobic microbial community.
Fig. 4: Proposed biotransformation pathways for CTFE3 and CTFE4.
Fig. 5: Biotransformation of Cl-terminal PFCAs by the anaerobic microbial community.
Fig. 6: Biotransformation of C2 and C3 chlorinated fluorocarboxylic acids and their H-substituted counterparts by the anaerobic microbial community.
Fig. 7: CTFE4 defluorination in subcultures of the anaerobic communities, the isolated colony and the pure cultures.

Similar content being viewed by others

Data availability

The metagenomic sequencing dataset has been deposited in the Sequence Read Archive under accession number PRJNA838587. Source data are provided with this paper. The draft genomes of the two dominant bacterial species in the isolated defluorinating colonies have been deposited in GenBank under the accession numbers JAMHFZ000000000 and JAMHGA000000000. All other data supporting the findings in this study are available within the paper and its Supplementary Information. Source data are provided with this paper.

References

  1. Dolbier, W. R. Fluorine chemistry at the millennium. J. Fluor. Chem. 126, 157–163 (2005).

    Article  CAS  Google Scholar 

  2. Lohmann, R. et al. Are fluoropolymers really of low concern for human and environmental health and separate from other PFAS. Environ. Sci. Technol. 54, 12820–12828 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Evich, M. G. et al. Per- and polyfluoroalkyl substances in the environment. Science 375, eabg9065 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Xiao, F. Emerging poly- and perfluoroalkyl substances in the aquatic environment: a review of current literature. Water Res. 124, 482–495 (2017).

    Article  CAS  PubMed  Google Scholar 

  5. Kotthoff, M. & Bucking, M. Four chemical trends will shape the next decade’s directions in perfluoroalkyl and polyfluoroalkyl substances research. Front. Chem. 6, 103 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Dams, R. & Hintzer, K. in Fluorinated Polymers: Applications Vol. 2 1–31 (The Royal Society of Chemistry, 2017).

  7. Vanbrocklin, C. Military applications of chlorotrifluoroethylene oligomer base nonflammable hydraulic fluid. J. Fire Sci. 11, 232–241 (1993).

    Article  CAS  Google Scholar 

  8. Gschweder, L., Mattie, D., Syder, C., Warer, W. & van Brocklin, C. Chlorotrifluoroethylene oligomer based nonflammable hydraulic fluid. 1 Fluid, additive, and elastomer development. J. Synth. Lubr. 9, 187–203 (1992).

    Article  Google Scholar 

  9. Ellis, D. A., Mabury, S. A., Martin, J. W. & Muir, D. C. Thermolysis of fluoropolymers as a potential source of halogenated organic acids in the environment. Nature 412, 321–324 (2001).

    Article  CAS  PubMed  Google Scholar 

  10. Myers, A. L., Jobst, K. J., Mabury, S. A. & Reiner, E. J. Using mass defect plots as a discovery tool to identify novel fluoropolymer thermal decomposition products. J. Mass Spectrom. 49, 291–296 (2014).

    Article  CAS  PubMed  Google Scholar 

  11. Dias, J. et al. Thermal degradation behavior of ionic liquid/fluorinated polymer composites: effect of polymer type and ionic liquid anion and cation. Polymer 229, 123995 (2021).

    Article  CAS  Google Scholar 

  12. DelRaso, N. J., Auten, K. L., Higman, H. C. & Leahy, H. F. Evidence of hepatic conversion of C6 and C8 chlorotrifluoroethylene (CTFE) oligomers to their corresponding CTFE acids. Toxicol. Lett. 59, 41–49 (1991).

    Article  CAS  PubMed  Google Scholar 

  13. Brashear, W. T., Greene, R. J. & Mahle, D. A. Structural determination of the carboxylic acid metabolites of polychlorotrifluoroethylene. Xenobiotica 22, 499–506 (1992).

    Article  CAS  PubMed  Google Scholar 

  14. Song, X., Vestergren, R., Shi, Y., Huang, J. & Cai, Y. Emissions, transport, and fate of emerging per- and polyfluoroalkyl substances from one of the major fluoropolymer manufacturing facilities in China. Environ. Sci. Technol. 52, 9694–9703 (2018).

    Article  CAS  PubMed  Google Scholar 

  15. Fujiwara, M., Jodry, J. J. & Narizuka, S. Process for producing alkoxycarbonylfluoroalkanesulfonates. US patent US20080108846A1 (2008).

  16. Yin, H., Anders, M. W. & Jones, J. P. Metabolism of 1,2-dichloro-1-fluoroethane and 1-fluoro-1,2,2-trichloroethane: electronic factors govern the regioselectivity of cytochrome P450-dependent oxidation. Chem. Res. Toxicol. 9, 50–57 (1996).

    Article  CAS  PubMed  Google Scholar 

  17. Harris, J. W. & Anders, M. W. Metabolism of the hydrochlorofluorocarbon 1,2-dichloro-1,1-difluoroethane. Chem. Res. Toxicol. 4, 180–186 (1991).

    Article  CAS  PubMed  Google Scholar 

  18. Liu, J. & Mejia Avendano, S. Microbial degradation of polyfluoroalkyl chemicals in the environment: a review. Environ. Int. 61, 98–114 (2013).

    Article  CAS  PubMed  Google Scholar 

  19. Yu, Y. et al. Microbial cleavage of C–F bonds in two C6 per- and polyfluorinated compounds via reductive defluorination. Environ. Sci. Technol. 54, 14393–14402 (2020).

    Article  CAS  PubMed  Google Scholar 

  20. Yu, Y. et al. Microbial defluorination of unsaturated per- and polyfluorinated carboxylic acids under anaerobic and aerobic conditions: a structure specificity study. Environ. Sci. Technol. 56, 4894–4904 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wackett, L. P. Nothing lasts forever: understanding microbial biodegradation of polyfluorinated compounds and perfluorinated alkyl substances. Microb. Biotechnol. 15, 773–792 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Adrian, L. & Löffler, F. E. Organohalide-Respiring Bacteria (Springer, 2016).

  23. Zhang, B. et al. Novel and legacy poly- and perfluoroalkyl substances (PFASs) in indoor dust from urban, industrial, and e-waste dismantling areas: the emergence of PFAS alternatives in China. Environ. Pollut. 263, 114461 (2020).

    Article  CAS  PubMed  Google Scholar 

  24. Liu, W. et al. Atmospheric chlorinated polyfluorinated ether sulfonate and ionic perfluoroalkyl acids in 2006 to 2014 in Dalian, China. Environ. Toxicol. Chem. 36, 2581–2586 (2017).

    Article  CAS  PubMed  Google Scholar 

  25. Wang, Y. et al. Suspect and nontarget screening of per- and polyfluoroalkyl substances in wastewater from a fluorochemical manufacturing park. Environ. Sci. Technol. 52, 11007–11016 (2018).

    Article  CAS  PubMed  Google Scholar 

  26. Liu, Y., Qian, M., Ma, X., Zhu, L. & Martin, J. W. Nontarget mass spectrometry reveals new perfluoroalkyl substances in fish from the Yangtze River and Tangxun Lake, China. Environ. Sci. Technol. 52, 5830–5840 (2018).

    Article  CAS  PubMed  Google Scholar 

  27. Washington, J. W. et al. Nontargeted mass-spectral detection of chloroperfluoropolyether carboxylates in New Jersey soils. Science 368, 1103–1107 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. MacInnis, J. J., Lehnherr, I., Muir, D. C. G., Quinlan, R. & De Silva, A. O. Characterization of perfluoroalkyl substances in sediment cores from High and Low Arctic lakes in Canada. Sci. Total Environ. 666, 414–422 (2019).

    Article  CAS  PubMed  Google Scholar 

  29. Lin, Y., Ruan, T., Liu, A. & Jiang, G. Identification of novel hydrogen-substituted polyfluoroalkyl ether sulfonates in environmental matrices near metal-plating facilities. Environ. Sci. Technol. 51, 11588–11596 (2017).

    Article  CAS  PubMed  Google Scholar 

  30. Yi, S., Zhu, L. & Mabury, S. A. First report on in vivo pharmacokinetics and biotransformation of chlorinated polyfluoroalkyl ether sulfonates in rainbow trout. Environ. Sci. Technol. 54, 345–354 (2020).

    Article  CAS  PubMed  Google Scholar 

  31. Yi, S., Yang, D., Zhu, L. & Mabury, S. A. Significant reductive transformation of 6:2 chlorinated polyfluorooctane ether sulfonate to form hydrogen-substituted polyfluorooctane ether sulfonate and their toxicokinetics in male Sprague–Dawley rats. Environ. Sci. Technol. 56, 6123–6132 (2021).

    Article  PubMed  Google Scholar 

  32. Lieberman, I. & Barker, H. A. β-Keto acid formation and decomposition by preparations of Clostridium kluyveri. J. Bacteriol. 68, 329–333 (1954).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Buschmann, J., Angst, W. & Schwarzenbach, R. P. Iron porphyrin and cysteine mediated reduction of ten polyhalogenated methanes in homogeneous aqueous solution: product analyses and mechanistic considerations. Environ. Sci. Technol. 33, 1015–1020 (1999).

    Article  CAS  Google Scholar 

  34. Che, S. et al. Structure-specific aerobic defluorination of short-chain fluorinated carboxylic acids by activated sludge communities. Environ. Sci. Technol. Lett. 8, 668–674 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Chen, G. et al. Anaerobic microbial metabolism of dichloroacetate. mBio https://doi.org/10.1128/mBio.00537-21 (2021).

  36. Möller, B., Oßmer, R., Howard, B. H., Gottschalk, G. & Hippe, H. Sporomusa, a new genus of gram-negative anaerobic bacteria including Sporomusa sphaeroides spec. nov. and Sporomusa ovata spec. nov. Arch. Microbiol. 139, 388–396 (1984).

    Article  Google Scholar 

  37. Temme, H. R., Carlson, A. & Novak, P. J. Presence, diversity, and enrichment of respiratory reductive dehalogenase and non-respiratory hydrolytic and oxidative dehalogenase genes in terrestrial environments. Front. Microbiol. 10, 1258 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Duhamel, M. & Edwards, E. A. Microbial composition of chlorinated ethene-degrading cultures dominated by Dehalococcoides. FEMS Microbiol. Ecol. 58, 538–549 (2006).

    Article  CAS  PubMed  Google Scholar 

  39. Baena, S. et al. Desulfovibrio aminophilus sp. nov., a novel amino acid degrading and sulfate reducing bacterium from an anaerobic dairy wastewater lagoon. Syst. Appl. Microbiol. 21, 498–504 (1998).

    Article  CAS  PubMed  Google Scholar 

  40. Yang, Y., Pesaro, M., Sigler, W. & Zeyer, J. Identification of microorganisms involved in reductive dehalogenation of chlorinated ethenes in an anaerobic microbial community. Water Res. 39, 3954–3966 (2005).

    Article  CAS  PubMed  Google Scholar 

  41. Water Quality—Determination of the Inhibitory Effect of Water Samples on the Light Emission of Vibrio fischeri (Luminescent Bacteria Test)—Part 3: Method Using Freeze-Dried Bacteria ISO 11348-3:2007 (ISO, 2007).

  42. Newton, S. et al. Novel polyfluorinated compounds identified using high resolution mass spectrometry downstream of manufacturing facilities near Decatur, Alabama. Environ. Sci. Technol. 51, 1544–1552 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Evich, M. G. et al. Environmental fate of Cl-PFPECAs: predicting the formation of PFAS transformation products in New Jersey soils. Environ. Sci. Technol. 56, 7779–7788 (2022).

    Article  CAS  PubMed  Google Scholar 

  44. Men, Y. et al. Sustainable syntrophic growth of Dehalococcoides ethenogenes strain 195 with Desulfovibrio vulgaris Hildenborough and Methanobacterium congolense: global transcriptomic and proteomic analyses. ISME J. 6, 410–421 (2012).

    Article  CAS  PubMed  Google Scholar 

  45. Schymanski, E. L. et al. Identifying small molecules via high resolution mass spectrometry: communicating confidence. Environ. Sci. Technol. 48, 2097–2098 (2014).

    Article  CAS  PubMed  Google Scholar 

  46. Tonomura, K., Futai, F., Tanabe, O. & Yamakoka, T. Defluorination of monofluoroacetate by bacteria. Part I. Isolation of bacteria and their activity of defluorination. Agric. Biol. Chem. 29, 124–128 (1965).

    CAS  Google Scholar 

  47. Davis, C. K., Webb, R. I., Sly, L. I., Denman, S. E. & McSweeney, C. S. Isolation and survey of novel fluoroacetate-degrading bacteria belonging to the phylum Synergistetes. FEMS Microbiol. Ecol. 80, 671–684 (2012).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Strategic Environmental Research and Development Program (project no. ER20-1541, for B.J., Y.Y., J.G., J.L. and Y.M.) and the National Institute of Environmental Health Sciences (award no. R01ES032668, for H.L., S.C. and Y.M.). M. Elsner at the Technical University of Munich provided insightful discussion on the biodefluorination pathways.

Author information

Authors and Affiliations

  1. Department of Chemical and Environmental Engineering, University of California, Riverside, Riverside, CA, USA

    Bosen Jin, Huaqing Liu, Shun Che, Jinyu Gao, Yaochun Yu, Jinyong Liu & Yujie Men

  2. Department of Civil and Environmental Engineering, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Shun Che, Yaochun Yu & Yujie Men

Authors
  1. Bosen Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huaqing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shun Che
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jinyu Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yaochun Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jinyong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yujie Men
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Y.M. and B.J. conceived and designed the project, analysed the data and prepared the paper. B.J. conducted the anaerobic biotransformation experiments using the anaerobic microbial community and pure cultures and analysed the LC–HRMS/MS and sequencing data. S.C. performed the aerobic biotransformation experiments and contributed to the anaerobic biotransformation set-up. H.L. performed the anaerobic isolation and sample preparation for metagenomic sequencing. Y.Y. contributed to the analysis of the analytical and sequencing data. J.G. contributed to the calculation of the BDEs. J.L. contributed to the PFAS compound selection and mechanistic discussion.

Corresponding author

Correspondence to Yujie Men.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Water thanks the anonymous reviewers for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods, Tables 1–4 and Figs. 1–15.

Supplementary Data 1

Source data for supplementary figures.

Source data

Source Data Fig. 1

Statistical source data.

Source Data Fig. 2

Statistical source data.

Source Data Fig. 3

Statistical source data.

Source Data Fig. 5

Statistical source data.

Source Data Fig. 6

Statistical source data.

Source Data Fig. 7

Statistical source data.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jin, B., Liu, H., Che, S. et al. Substantial defluorination of polychlorofluorocarboxylic acids triggered by anaerobic microbial hydrolytic dechlorination. Nat Water 1, 451–461 (2023). https://doi.org/10.1038/s44221-023-00077-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s44221-023-00077-6

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing