Cited by 52Per- and polyfluoroalkyl substances researchEnvironmental Chemistry and AnalysisWater Treatment and Disinfection

Nitrifying Microorganisms Linked to Biotransformation of Perfluoroalkyl Sulfonamido Precursors from Legacy Aqueous Film-Forming Foams

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Ruyle, Bridger J., Schultes, Lara, Akob, Denise M., Harris, Cassandra R., Lorah, Michelle M., Vojta, Simon, Becanova, Jitka, McCann, Shelley +5 more·2023·Environmental Science & Technology

Abstract

High Resolution Image Download MS PowerPoint Slide Drinking water supplies across the United States have been contaminated by firefighting and fire-training activities that use aqueous film-forming foams (AFFF) containing per- and polyfluoroalkyl substances (PFAS). Much of the AFFF is manufactured using electrochemical fluorination by 3M. Precursors with six perfluorinated carbons (C6) and non-fluorinated amine substituents make up approximately one-third of the PFAS in 3M AFFF. C6 precursors can be transformed through nitrification (microbial oxidation) of amine moieties into perfluorohexane sulfonate (PFHxS), a compound of regulatory concern. Here, we report biotransformation of the most abundant C6 sulfonamido precursors in 3M AFFF with available commercial standards (FHxSA, PFHxSAm, and PFHxSAmS) in microcosms representative of the groundwater/surface water boundary. Results show rapid (<1 day) biosorption to living cells by precursors but slow biotransformation into PFHxS (1–100 pM day –1 ). The transformation pathway includes one or two nitrification steps and is supported by the detection of key intermediates using high-resolution mass spectrometry. Increasing nitrate concentrations and total abundance of nitrifying taxa occur in parallel with precursor biotransformation. Together, these data provide multiple lines of evidence supporting microbially limited biotransformation of C6 sulfonamido precursors involving ammonia-oxidizing archaea ( Nitrososphaeria ) and nitrite-oxidizing bacteria ( Nitrospina ). Further elucidation of interrelationships between precursor biotransformation and nitrogen cycling in ecosystems would help inform site remediation efforts.

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Crossref · 10.1021/acs.est.2c07178

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  • Slow precursor biotransformation rates help explain why previous microcosm studies have observed minimal production of terminal PFAS and have not been able to quantify rates.

    “Slow precursor biotransformation rates help explain why previous microcosm studies (conducted over weeks/months timescales) have observed minimal production of terminal PFAS and have not been able to quantify rates.24,45,46”

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  1. [2]Sunderland EM; Hu XC; Dassuncao C; Tokranov AK; Wagner CC; Allen JG A Review of the Pathways of Human Exposure to Poly- and Perfluoroalkyl Substances (PFASs) and Present Understanding of Health Effects. Journal of Exposure Science & Environmental Epidemiology 2019, 29 (2), 131– 147. 10.1038/s41370-018-0094-1. 30470793 PMC6380916 · DOI · Paper page
  2. [3]Fenton SE; Ducatman A; Boobis A; DeWitt JC; Lau C; Ng C; Smith JS; Roberts SM Per- and Polyfluoroalkyl Substance Toxicity and Human Health Review: Current State of Knowledge and Strategies for Informing Future Research. Environmental Toxicology and Chemistry 2021, 40 (3), 606– 630. 10.1002/etc.4890. 33017053 PMC7906952 · DOI · Paper page
  3. [5]Barzen-Hanson KA; Roberts SC; Choyke S; Oetjen K; McAlees A; Riddell N; McCrindle R; Ferguson PL; Higgins CP; Field JA Discovery of 40 Classes of Per- and Polyfluoroalkyl Substances in Historical Aqueous Film-Forming Foams (AFFFs) and AFFF-Impacted Groundwater. Environmental Science & Technology 2017, 51 (4), 2047– 2057. 10.1021/acs.est.6b05843. 28098989 · DOI · Paper page
  4. [7]Ruyle BJ; Thackray CP; McCord JP; Strynar MJ; Mauge-Lewis KA; Fenton SE; Sunderland EM Reconstructing the Composition of Per- and Polyfluoroalkyl Substances in Contemporary Aqueous Film-Forming Foams. Environ. Sci. Technol. Lett. 2021, 8 (1), 59– 65. 10.1021/acs.estlett.0c00798. 33628855 PMC7898139 · DOI · Paper page
  5. [8]Tokranov AK; LeBlanc DR; Pickard HM; Ruyle BJ; Barber LB; Hull RB; Sunderland EM; Vecitis CD Surface-Water/Groundwater Boundaries Affect Seasonal PFAS Concentrations and PFAA Precursor Transformations. Environ. Sci.: Processes Impacts 2021, 10.1039.D1EM00329A. 10.1039/D1EM00329A. PMC8673475 34779453 · DOI · Paper page
  6. [9]Hu XC; Andrews DQ; Lindstrom AB; Bruton TA; Schaider LA; Grandjean P; Lohmann R; Carignan CC; Blum A; Balan SA; Higgins CP; Sunderland EM Detection of Poly- and Perfluoroalkyl Substances (PFASs) in U.S. Drinking Water Linked to Industrial Sites, Military Fire Training Areas, and Wastewater Treatment Plants. Environmental Science & Technology Letters 2016, 3 (10), 344– 350. 10.1021/acs.estlett.6b00260. 27752509 PMC5062567 · DOI · Paper page
  7. [11]Place BJ; Field JA Identification of Novel Fluorochemicals in Aqueous Film-Forming Foams Used by the US Military. Environmental Science & Technology 2012, 46 (13), 7120– 7127. 10.1021/es301465n. 22681548 PMC3390017 · DOI · Paper page
  8. [12]Cook EK; Olivares CI; Antell EH; Yi S; Nickerson A; Choi YJ; Higgins CP; Sedlak DL; Alvarez-Cohen L Biological and Chemical Transformation of the Six-Carbon Polyfluoroalkyl Substance N-Dimethyl Ammonio Propyl Perfluorohexane Sulfonamide (AmPr-FHxSA). Environ. Sci. Technol. 2022. 10.1021/acs.est.2c00261. 36257682 · DOI
  9. [13]D’Agostino LA; Mabury SA Certain Perfluoroalkyl and Polyfluoroalkyl Substances Associated with Aqueous Film Forming Foam Are Widespread in Canadian Surface Waters. Environmental Science & Technology 2017, 51 (23), 13603– 13613. 10.1021/acs.est.7b03994. 29110476 · DOI · Paper page
  10. [14]Liu M; Munoz G; Vo Duy S; Sauvé S; Liu J Per- and Polyfluoroalkyl Substances in Contaminated Soil and Groundwater at Airports: A Canadian Case Study. Environ. Sci. Technol. 2022, 56 (2), 885– 895. 10.1021/acs.est.1c04798. 34967613 · DOI
  11. [16]Nickerson A; Rodowa AE; Adamson DT; Field JA; Kulkarni PR; Kornuc JJ; Higgins CP Spatial Trends of Anionic, Zwitterionic, and Cationic PFASs at an AFFF-Impacted Site. Environ. Sci. Technol. 2021, 55 (1), 313– 323. 10.1021/acs.est.0c04473. 33351591 · DOI · Paper page
  12. [17]Ruyle BJ; Pickard HM; LeBlanc DR; Tokranov AK; Thackray CP; Hu XC; Vecitis CD; Sunderland EM Isolating the AFFF Signature in Coastal Watersheds Using Oxidizable PFAS Precursors and Unexplained Organofluorine. Environ. Sci. Technol. 2021, 55 (6), 3686– 3695. 10.1021/acs.est.0c07296. 33667081 PMC11082878 · DOI · Paper page
  13. [18]Choi YJ; Helbling DE; Liu J; Olivares CI; Higgins CP Microbial Biotransformation of Aqueous Film-Forming Foam Derived Polyfluoroalkyl Substances. Science of The Total Environment 2022, 824, 153711. 10.1016/j.scitotenv.2022.153711. 35149076 · DOI · Paper page
  14. [20]Liu M; Munoz G; Vo Duy S; Sauvé S; Liu J Stability of Nitrogen-Containing Polyfluoroalkyl Substances in Aerobic Soils. Environ. Sci. Technol. 2021, 55 (8), 4698– 4708. 10.1021/acs.est.0c05811. 33739092 · DOI
  15. [21]O’Carroll DM; Jeffries TC; Lee MJ; Le ST; Yeung A; Wallace S; Battye N; Patch DJ; Mane MJ Developing a Roadmap to Determine Per- and Polyfluoroalkyl Substances-Microbial Population Interactions. Science of The Total Environment 2020, 712, 10. 10.1016/j.scitotenv.2019.135994. 31931194 · DOI
  16. [22]Tang Z; Song X; Xu M; Yao J; Ali M; Wang Q; Zeng J; Ding X; Wang C; Zhang Z; Liu X Effects of Co-Occurrence of PFASs and Chlorinated Aliphatic Hydrocarbons on Microbial Communities in Groundwater: A Field Study. Journal of Hazardous Materials 2022, 435, 128969. 10.1016/j.jhazmat.2022.128969. 35472535 · DOI
  17. [25]Harding-Marjanovic KC; Houtz EF; Yi S; Field JA; Sedlak DL; Alvarez-Cohen L Aerobic Biotransformation of Fluorotelomer Thioether Amido Sulfonate (Lodyne) in AFFF-Amended Microcosms. Environ. Sci. Technol. 2015, 49 (13), 7666– 7674. 10.1021/acs.est.5b01219. 26042823 · DOI · Paper page
  18. [26]Lichstein HC; Soule MH Studies of the Effect of Sodium Azide on Microbic Growth and Respiration. Journal of Bacteriology 1944, 47 (3), 221– 230. 10.1128/jb.47.3.221-230.1944. 16560767 PMC373901 · DOI
  19. [27]Hammes F; Vital M; Egli T Critical Evaluation of the Volumetric “Bottle Effect” on Microbial Batch Growth. Applied and Environmental Microbiology 2010, 76 (4), 1278– 1281. 10.1128/AEM.01914-09. 20023110 PMC2820953 · DOI
  20. [29]Jian C; Luukkonen P; Yki-Järvinen H; Salonen A; Korpela K Quantitative PCR Provides a Simple and Accessible Method for Quantitative Microbiota Profiling. PLOS ONE 2020, 15 (1), e0227285. 10.1371/journal.pone.0227285. 31940382 PMC6961887 · DOI · Paper page
  21. [30]Tettamanti Boshier FA; Srinivasan S; Lopez A; Hoffman NG; Proll S; Fredricks DN; Schiffer JT Complementing 16S RRNA Gene Amplicon Sequencing with Total Bacterial Load To Infer Absolute Species Concentrations in the Vaginal Microbiome. mSystems 2020, 5 (2), e00777– 19. 10.1128/mSystems.00777-19. 32265316 PMC7141891 · DOI · Paper page
  22. [31]Epp Schmidt D; Dlott G; Cavigelli M; Yarwood S; Maul JE Soil Microbiomes in Three Farming Systems More Affected by Depth than Farming System. Applied Soil Ecology 2022, 173, 104396. 10.1016/j.apsoil.2022.104396. · DOI
  23. [32]Caporaso JG; Lauber CL; Walters WA; Berg-Lyons D; Huntley J; Fierer N; Owens SM; Betley J; Fraser L; Bauer M; Gormley N; Gilbert JA; Smith G; Knight R Ultra-High-Throughput Microbial Community Analysis on the Illumina HiSeq and MiSeq Platforms. ISME J 2012, 6 (8), 1621– 1624. 10.1038/ismej.2012.8. 22402401 PMC3400413 · DOI · Paper page
  24. [33]Apprill A; McNally S; Parsons R; Weber L Minor Revision to V4 Region SSU RRNA 806R Gene Primer Greatly Increases Detection of SAR11 Bacterioplankton. Aquatic Microbial Ecology 2015, 75 (2), 129– 137. 10.3354/ame01753. · DOI · Paper page
  25. [34]Parada AE; Needham DM; Fuhrman JA Every Base Matters: Assessing Small Subunit RRNA Primers for Marine Microbiomes with Mock Communities, Time Series and Global Field Samples. Environmental Microbiology 2016, 18 (5), 1403– 1414. 10.1111/1462-2920.13023. 26271760 · DOI
  26. [35]Walters W; Hyde ER; Berg-Lyons D; Ackermann G; Humphrey G; Parada A; Gilbert JA; Jansson JK; Caporaso JG; Fuhrman JA; Apprill A; Knight R Improved Bacterial 16S RRNA Gene (V4 and V4–5) and Fungal Internal Transcribed Spacer Marker Gene Primers for Microbial Community Surveys. mSystems 2015, 1 (1), e00009– 15. 10.1128/mSystems.00009-15. 27822518 PMC5069754 · DOI
  27. [36]Akob DM; Küsel K Where Microorganisms Meet Rocks in the Earth’s Critical Zone. Biogeosciences 2011, 8 (12), 3531– 3543. 10.5194/bg-8-3531-2011. · DOI
  28. [37]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 Introducing Mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Applied and Environmental Microbiology 2009, 75 (23), 7537– 7541. 10.1128/AEM.01541-09. 19801464 PMC2786419 · DOI
  29. [38]Pruesse E; Quast C; Knittel K; Fuchs BM; Ludwig W; Peplies J; Glöckner FO SILVA: A Comprehensive Online Resource for Quality Checked and Aligned Ribosomal RNA Sequence Data Compatible with ARB. Nucleic Acids Res 2007, 35 (21), 7188– 7196. 10.1093/nar/gkm864. 17947321 PMC2175337 · DOI
  30. [39]Quast C; Pruesse E; Yilmaz P; Gerken J; Schweer T; Yarza P; Peplies J; Glöckner FO The SILVA Ribosomal RNA Gene Database Project: Improved Data Processing and Web-Based Tools. Nucleic Acids Res 2013, 41 (Database issue), D590– D596. 10.1093/nar/gks1219. 23193283 PMC3531112 · DOI · Paper page
  31. [41]Schwarzenbach RP; Gschwend PM; Imboden DM Environmental Organic Chemistry, 3rd ed.; John Wiley & Sons, Inc.: Hoboken, New Jersey, 2017.
  32. [42]Plazinski W; Rudzinski W; Plazinska A Theoretical Models of Sorption Kinetics Including a Surface Reaction Mechanism: A Review. Advances in Colloid and Interface Science 2009, 152 (1), 2– 13. 10.1016/j.cis.2009.07.009. 19735907 · DOI
  33. [44]Foreman-Mackey D; Hogg DW; Lang D; Goodman J Emcee: The MCMC Hammer. arXiv:1202.3665 [astro-ph, physics:physics, stat] 2013. 10.1086/670067. · DOI
  34. [46]Fitzgerald NJM; Wargenau A; Sorenson C; Pedersen J; Tufenkji N; Novak PJ; Simcik MF Partitioning and Accumulation of Perfluoroalkyl Substances in Model Lipid Bilayers and Bacteria. Environ. Sci. Technol. 2018, 52 (18), 10433– 10440. 10.1021/acs.est.8b02912. 30148610 · DOI
  35. [48]Qin W; Martens-Habbena W; Kobelt JN; Stahl DA Candidatus Nitrosopumilales. In Bergey’s Manual of Systematics of Archaea and Bacteria; John Wiley & Sons, Ltd, 2016; pp 1– 2. 10.1002/9781118960608.obm00122. · DOI
  36. [49]Stieglmeier M; Klingl A; Alves RJE; Rittmann SK-MR; Melcher M; Leisch N; Schleper C 2014. Nitrososphaera Viennensis Gen. Nov., Sp. Nov., an Aerobic and Mesophilic, Ammonia-Oxidizing Archaeon from Soil and a Member of the Archaeal Phylum Thaumarchaeota. International Journal of Systematic and Evolutionary Microbiology 2014, 64 (Pt_8), 2738– 2752. 10.1099/ijs.0.063172-0. 24907263 PMC4129164 · DOI
  37. [51]Shaw DMJ; Munoz G; Bottos EM; Duy SV; Sauvé S; Liu J; Van Hamme JD Degradation and Defluorination of 6:2 Fluorotelomer Sulfonamidoalkyl Betaine and 6:2 Fluorotelomer Sulfonate by Gordonia Sp. Strain NB4–1Y under Sulfur-Limiting Conditions. Science of The Total Environment 2019, 647, 690– 698. 10.1016/j.scitotenv.2018.08.012. 30092525 · DOI · Paper page
  38. [52]Kim MH; Wang N; McDonald T; Chu K-H Biodefluorination and Biotransformation of Fluorotelomer Alcohols by Two Alkane-Degrading Pseudomonas Strains. Biotechnology and Bioengineering 2012, 109 (12), 3041– 3048. 10.1002/bit.24561. 22614340 · DOI · Paper page
  39. [53]Kim MH; Wang N; Chu KH 6:2 Fluorotelomer Alcohol (6:2 FTOH) Biodegradation by Multiple Microbial Species under Different Physiological Conditions. Appl Microbiol Biotechnol 2014, 98 (4), 1831– 1840. 10.1007/s00253-013-5131-3. 23907259 · DOI · Paper page
  40. [54]Fox BG; Borneman JG; Wackett LP; Lipscomb JD Haloalkene Oxidation by the Soluble Methane Monooxygenase from Methylosinus Trichosporium OB3b: Mechanistic and Environmental Implications. Biochemistry 1990, 29 (27), 6419– 6427. 10.1021/bi00479a013. 2207083 · DOI
  41. [55]Yin T; Te SH; Reinhard M; Yang Y; Chen H; He Y; Gin KY-H Biotransformation of Sulfluramid (N-Ethyl Perfluorooctane Sulfonamide) and Dynamics of Associated Rhizospheric Microbial Community in Microcosms of Wetland Plants. Chemosphere 2018, 211, 379– 389. 10.1016/j.chemosphere.2018.07.157. 30077934 · DOI · Paper page
  42. [56]Yin T; Tran NH; Huiting C; He Y; Gin KY-H Biotransformation of Polyfluoroalkyl Substances by Microbial Consortia from Constructed Wetlands under Aerobic and Anoxic Conditions. Chemosphere 2019, 233, 101– 109. 10.1016/j.chemosphere.2019.05.227. 31170581 · DOI

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Authors
Ruyle, B. J., Schultes, L., Akob, D. M., Harris, C. R., Lorah, M. M., Vojta, S., Becanova, J., McCann, S., Pickard, H. M., Pearson, A., Lohmann, R., Vecitis, C. D., & Sunderland, E. M.
Affiliations
  • Harvard University (US)
  • United States Geological Survey (US)
  • Maryland-Delaware-D.C. Water Science Center (US)
  • Graduate School of Oceanography, University of Rhode Island, Narragansett, Rhode Island 02882, United States
  • University of Rhode Island (US)
Corresponding author
Ruyle, Bridger J.
Venue
Environmental Science & Technology
Published
2023-03-27
Volume
57
Issue
14
Pages
5592-5602
ISSN
  • 0013-936X (ISSN-L)
  • 1520-5851
OpenAlex
W4360990253
Cited by
52
References
9
Citations by year
2026: 15 · 2025: 18 · 2024: 16 · 2023: 3
FWCI
4.48
Type
journal article
Language
en
Open access
Locations
  • Environmental Science & Technology (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Journal of Media Literacy Education (submittedVersion, cc-by-nc-nd)
Funders
  • National Institute of Environmental Health Sciences (P42ES027706)
  • U.S. Department of Defense (SERDP ER18-1280)
  • U.S. Geological Survey
Topics
  • Physical Sciences › Environmental Science › Environmental Chemistry › Per- and polyfluoroalkyl substances research
  • Physical Sciences › Environmental Science › Environmental Chemistry › Environmental Chemistry and Analysis
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Water Treatment and Disinfection
Keywords
aqueous film-forming foam, PFAS contamination, nitrification, PFHxS, biotransformation, biosorption, ammonia-oxidizing archaea, Nitrososphaeria, nitrite-oxidizing bacteria, Nitrospina, groundwater contamination, nitrogen cycling, firefighting foam, nitrate, remediation
MeSH terms
Alkanesulfonates, Biotransformation, Fluorocarbons, Water Pollutants, Chemical, Ecosystem, Groundwater

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