Biotransformation of 6:2 fluorotelomer sulfonate (6:2 FTS) in sulfur-rich media by Trametopsis cervina

Highlights

● Biotransformation of 6:2 fluorotelomer sulfonate (6:2 FTS) can occur in S-rich media.

● Both stable and intermediate products were identified from the biotransformation of 6:2 FTS.

● Mass loss due to volatile intermediate PFASs can be theoretically estimated.

● Volatile PFAS may represent a significant portion of 6:2 FTS transformation products.

Abstract

Biotransformation of 6:2 fluorotelomer sulfonate (6:2 FTS) by two species of white-rot fungi, Pleurotus ostreatus (P. ostreatus) and Trametopsis cervina (T. cervina), was investigated in a sulfur-rich medium designed to stimulate production of lignin-degrading enzymes. Degradation of 6:2 FTS was observed by T. cervina over the study period of 30 d, but not by P. ostreatus. Biotransformation rates were comparable to those found in other studies investigating mixed culture degradation in non-sulfur limiting media, with approximately 50 mol% of applied 6:2 FTS removed after 30 d. Stable transformation products were short-chain perfluorocarboxylic acids (PFCAs), including PFHxA (2.27 mol%), PFPeA (0.24 mol%), and PFBA (0.28 mol%). The main intermediate products include 5:2 sFTOH (16.3 mol%) and 5:3 FTCA (2.99 mol%), while 6:2 FTCA, 6:2 FTuCA, and 5:2 ketone were also identified at low levels. Approximately 60 mol% of detected products were assigned to the major pathway to 5:2 ketone, and 40 mol% were assigned to the minor pathway to 5:3 FTCA. The overall molar balance was found to decrease to 75 mol% by Day 30, however, was closed to near 95 mol% with a theoretical estimation for the volatile intermediates in the headspace, 5:2 ketone and 5:2 sFTOH. The different capabilities of the two white-rot fungal species for 6:2 FTS biotransformation in sulfur-rich media suggest that the enzyme processes of T. cervina to de-sulfonate 6:2 FTS may be unrelated to sulfur metabolism.

Keywords

White-rot fungus / 6:2 fluorotelomer sulfonate (6:2 FTS) / Biotransformation / Sulfur-rich medium / Intermediate products

References

[1] Backe W J, Day T C, Field J A. (2013). Zwitterionic, cationic, and anionic fluorinated chemicals in aqueous film forming foam formulations and groundwater from U.S. military bases by nonaqueous large-volume injection HPLC-MS/MS. Environmental Science & Technology, 47(10): 5226–5234

[2] Barzen-Hanson K A, Roberts S C, Choyke S, Oetjen K, McAlees A, Riddell N, McCrindle R, Ferguson P L, Higgins C P, Field J A. (2017). Discovery of 40 Classes of per- and polyfluoroalkyl substances in historical aqueous film-forming foams (AFFFs) and AFFF-impacted groundwater. Environmental Science & Technology, 51(4): 2047–2057

[3] BuckR C (2015). Toxicology data for alternative “short-chain” fluorinated substances. DeWitt J C, ed. Toxicological Effects of Perfluoroalkyl and Polyfluoroalkyl Substances, Molecular and Integrative Toxicology. Cham: Springer International Publishing 10.1007/978-3-319-15518-0_17

[4] Cachet C, Keddam M, Mariotte V, Wiart R. (1993). Adsorption of perfluorinated surfactants on gold electrodes—II. Behaviour of ionic compounds. Electrochimica Acta, 38(15): 2203–2208

[5] Cachet C, Keddam M, Mariotte V, Wiart R. (1994). Influence of perfluorinated and hydrogenated surfactants upon hydrogen evolution on gold electrodes. Electrochimica Acta, 39(18): 2743–2750

[6] Christopher L P, Yao B, Ji Y. (2014). Lignin biodegradation with laccase-mediator systems. Frontiers in Energy Research, 2: 12

[7] Cui D, Li X, Quinete N. (2020). Occurrence, fate, sources and toxicity of PFAS: What we know so far in Florida and major gaps. Trends in Analytical Chemistry, 130: 115976

[8] D’Agostino L A, Mabury S A. (2017). Certain perfluoroalkyl and polyfluoroalkyl substances associated with aqueous film forming foam are widespread in Canadian surface waters. Environmental Science & Technology, 51(23): 13603–13613

[9] DuPont (2010). DuPont Surface Protection Solutions. DuPontTM Capstone® Repellent and Surfactants Product Stewardship Detail. Wilmington: DuPont Experimental Station

[10] Field J A, Seow J. (2017). Properties, occurrence, and fate of fluorotelomer sulfonates. Critical Reviews in Environmental Science and Technology, 47(8): 643–691

[11] FrancoP C I, Shiraishi I S, DekkerR F H, Barbosa-DekkerA M, Borsato D, AngilelliK B, EvaristoG P C, Simionato J I, DanielJ F S (2023). Optimization of laccase production by Pleurotus ostreatus Florida and evaluation of metabolites generated during Kraft lignin biotransformation. Waste Biomass Valor 14: 2589–2597 10.1007/s12649-022-02029-9

[12] Hamid H, Li L Y, Grace J R. (2020a). Formation of perfluorocarboxylic acids from 6:2 fluorotelomer sulfonate (6:2 FTS) in landfill leachate: role of microbial communities. Environmental Pollution, 259: 113835

[13] Hamid H, Li L Y, Grace J R. (2020b). Effect of substrate concentrations on aerobic biotransformation of 6:2 fluorotelomer sulfonate (6:2 FTS) in landfill leachate. Chemosphere, 261: 128108

[14] Hirano T, Honda Y, Watanabe T, Kuwahara M. (2000). Degradation of bisphenol a by the lignin-degrading enzyme, manganese peroxidase, produced by the white-rot basidiomycete, Pleurotus ostreatus. Bioscience, Biotechnology, and Biochemistry, 64(9): 1958–1962

[15] Hoke R A, Ferrell B D, Ryan T, Sloman T L, Green J W, Nabb D L, Mingoia R, Buck R C, Korzeniowski S H. (2015). Aquatic hazard, bioaccumulation and screening risk assessment for 6:2 fluorotelomer sulfonate. Chemosphere, 128: 258–265

[16] Karp S G, Faraco V, Amore A, Birolo L, Giangrande C, Soccol V T, Pandey A, Soccol C R. (2012). Characterization of laccase isoforms produced by Pleurotus ostreatus in solid state fermentation of sugarcane bagasse. Bioresource Technology, 114: 735–739

[17] Kärrman A, Elgh-Dalgren K, Lafossas C, Møskeland T. (2011). Environmental levels and distribution of structural isomers of perfluoroalkyl acids after aqueous fire-fighting foam (AFFF) contamination. Environmental Chemistry, 8(4): 372

[18] KorzeniowskiS, CortinaT. (2008) Firefighting foams. KorzeniowskiS, BuchR C, Kempisty D M, et al. Ed. Perfluoroalkyl Substances in the Environment. Boca Raton: CRC Press

[19] KüesU (2015). Fungal enzymes for environmental management. Current Opinion in Biotechnology, 33, 268–278 10.1016/j.copbio.2015.03.006

[20] Kurwadkar S, Dane J, Kanel S R, Nadagouda M N, Cawdrey R W, Ambade B, Struckhoff G C, Wilkin R. (2022). Per- and polyfluoroalkyl substances in water and wastewater: a critical review of their global occurrence and distribution. Science of the Total Environment, 809: 151003

[21] Liu J, Wang N, Szostek B, Buck R C, Panciroli P K, Folsom P W, Sulecki L M, Bellin C A. (2010). Fluorotelomer alcohol aerobic biodegradation in soil and mixed bacterial culture. Chemosphere, 78(4): 437–444

[22] Liu M, Munoz G, Vo Duy S, Sauvé S, Liu J. (2022). Per- and polyfluoroalkyl substances in contaminated soil and groundwater at airports: a Canadian case study. Environmental Science & Technology, 56(2): 885–895

[23] Luo Q, Liang S, Huang Q. (2018a). Laccase induced degradation of perfluorooctanoic acid in a soil slurry. Journal of Hazardous Materials, 359: 241–247

[24] Luo Q, Wang Z, Feng M, Chiang D, Woodward D, Liang S, Lu J, Huang Q. (2017). Factors controlling the rate of perfluorooctanoic acid degradation in laccase-mediator systems: the impact of metal ions. Environmental Pollution, 224: 649–657

[25] Luo Q, Yan X, Lu J, Huang Q. (2018b). Perfluorooctanesulfonate degrades in a laccase-mediator system. Environmental Science & Technology, 52(18): 10617–10626

[26] Méndez V, Holland S, Bhardwaj S, McDonald J, Khan S, O’Carroll D, Pickford R, Richards S, O’Farrell C, Coleman N. . (2022). Aerobic biotransformation of 6:2 fluorotelomer sulfonate by Dietzia aurantiaca J3 under sulfur-limiting conditions. Science of the Total Environment, 829: 154587

[27] Merino N, Wang M, Ambrocio R, Mak K, O’Connor E, Gao A, Hawley E L, Deeb R A, Tseng L Y, Mahendra S. (2018). Fungal biotransformation of 6:2 fluorotelomer alcohol. Remediation Journal, 28(2): 59–70

[28] Moe M K, Huber S, Svenson J, Hagenaars A, Pabon M, Trümper M, Berger U, Knapen D, Herzke D. (2012). The structure of the fire fighting foam surfactant Forafac®1157 and its biological and photolytic transformation products. Chemosphere, 89(7): 869–875

[29] Novotný Č, Svobodová K, Erbanová P, Cajthaml T, Kasinath A, Lang E, Šašek V. (2004). Ligninolytic fungi in bioremediation: extracellular enzyme production and degradation rate. Soil Biology & Biochemistry, 36(10): 1545–1551

[30] Place B J, Field J A. (2012a). Identification of novel fluorochemicals in aqueous film-forming foams used by the US military. Environmental Science & Technology, 46(13): 7120–7127

[31] Place B J, Field J A. (2012b). Identification of novel fluorochemicals in aqueous film-forming foams used by the US military. Environmental Science & Technology, 46(13): 7120–7127

[32] Riaz R, Junaid M, Rehman M Y A, Iqbal T, Khan J A, Dong Y, Yue L, Chen Y, Xu N, Malik R N. (2023). Spatial distribution, compositional profile, sources, ecological and human health risks of legacy and emerging per- and polyfluoroalkyl substances (PFASs) in freshwater reservoirs of Punjab, Pakistan. Science of the Total Environment, 856: 159144

[33] Ritter S. (2010). Fluorochemicals go short. Chem. Eng. News Archive, 88: 12–17

[34] Ruan T, Szostek B, Folsom P W, Wolstenholme B W, Liu R, Liu J, Jiang G, Wang N, Buck R C. (2013). Aerobic soil biotransformation of 6:2 fluorotelomer iodide. Environmental Science & Technology, 47(20): 11504–11511

[35] Ruttkies C, Schymanski E L, Wolf S, Hollender J, Neumann S. (2016). MetFrag relaunched: incorporating strategies beyond in silico fragmentation. Journal of Cheminformatics, 8(1): 3

[36] Schultz M M, Barofsky D F, Field J A. (2004). Quantitative determination of fluorotelomer sulfonates in groundwater by LC MS/MS. Environmental Science & Technology, 38(6): 1828–1835

[37] Schwichtenberg T, Bogdan D, Carignan C C, Reardon P, Rewerts J, Wanzek T, Field J A. (2020). PFAS and dissolved organic carbon enrichment in surface water foams on a northern U.S. freshwater lake. Environmental Science & Technology, 54(22): 14455–14464

[38] Shakhova N. (2020). Revealing new active and biotechnologically perspective producers of oxidative and cellulolytic enzymes among pure cultures of xylotrophic agaricomycetes from the southern non-chernozem zone of the european part of Russia. Current Research in Environmental & Applied Mycology, 10(1): 113–119

[39] Shaw D M J, Munoz G, Bottos E M, Duy S V, Sauvé S, Liu J, Van Hamme J D. (2019). 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, 647: 690–698

[40] ShiY (2018). Bacterial desulfonation and defluorination of 6:2 fluorotelomer sulfonate (6:2 FTS). Thesis for the Master’s Degree. College Station: Texas A&M University

[41] Shojaei M, Kumar N, Chaobol S, Wu K, Crimi M, Guelfo J. (2021). Enhanced recovery of per- and polyfluoroalkyl substances (PFASs) from impacted soils using heat activated persulfate. Environmental Science & Technology, 55(14): 9805–9816

[42] Singh D, Chen S. (2008). The white-rot fungus Phanerochaete chrysosporium: conditions for the production of lignin-degrading enzymes. Applied Microbiology and Biotechnology, 81(3): 399–417

[43] Sista Kameshwar A K, Qin W. (2018). Comparative study of genome-wide plant biomass-degrading CAZymes in white rot, brown rot and soft rot fungi. Mycology, 9(2): 93–105

[44] Sunderland E M, Hu X C, Dassuncao C, Tokranov A K, Wagner C C, Allen J G. (2019). 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, 29(2): 131–147

[45] Tang A, Zhang X, Li R, Tu W, Guo H, Zhang Y, Li Z, Liu Y, Mai B. (2022). Spatiotemporal distribution, partitioning behavior and flux of per- and polyfluoroalkyl substances in surface water and sediment from Poyang Lake, China. Chemosphere, 295: 133855

[46] Tseng N, Wang N, Szostek B, Mahendra S. (2014). Biotransformation of 6:2 fluorotelomer alcohol (6:2 FTOH) by a wood-rotting fungus. Environmental Science & Technology, 48(7): 4012–4020

[47] Vaithanomsat P, Sangnam A, Boonpratuang T, Choeyklin R, Promkiam-on P, Chuntranuluck S, Kreetachat T. (2013). Wood degradation and optimized laccase production by resupinate white-rot fungi in northern Thailand: bioresources. Bioresource Technology, 8: 6342–6360

[48] Van Hamme J D, Bottos E M, Bilbey N J, Brewer S E. (2013). Genomic and proteomic characterization of Gordonia sp. NB4–1Y in relation to 6 : 2 fluorotelomer sulfonate biodegradation. Microbiology, 159(Pt_8): 1618–1628

[49] Vrsanska M, Voberkova S, Langer V, Palovcikova D, Moulick A, Adam V, Kopel P. (2016). Induction of laccase, lignin peroxidase and manganese peroxidase activities in white-rot fungi using copper complexes. Molecules, 21(11): 1553

[50] Wang N, Liu J, Buck R C, Korzeniowski S H, Wolstenholme B W, Folsom P W, Sulecki L M. (2011). 6:2 Fluorotelomer sulfonate aerobic biotransformation in activated sludge of waste water treatment plants. Chemosphere, 82(6): 853–858

[51] Wolf S, Schmidt S, Müller-Hannemann M, Neumann S. (2010). In silico fragmentation for computer assisted identification of metabolite mass spectra. BMC Bioinformatics, 11(1): 148

[52] Yang S H, Shi Y, Strynar M, Chu K H. (2022). Desulfonation and defluorination of 6:2 fluorotelomer sulfonic acid (6:2 FTSA) by Rhodococcus jostii RHA1: carbon and sulfur sources, enzymes, and pathways. Journal of Hazardous Materials, 423: 127052

[53] Yin T, Tran N H, Huiting C, He Y, Gin K Y H. (2019). Biotransformation of polyfluoroalkyl substances by microbial consortia from constructed wetlands under aerobic and anoxic conditions. Chemosphere, 233: 101–109

[54] Zhang S, Lu X, Wang N, Buck R. (2016). Biotransformation potential of 6:2 fluorotelomer sulfonate (6:2 FTSA) in aerobic and anaerobic sediment. Chemosphere, 154: 224–230

[55] Zhang S, Szostek B, McCausland P K, Wolstenholme B W, Lu X, Wang N, Buck R C. (2013). 6:2 and 8:2 Fluorotelomer alcohol anaerobic biotransformation in digester sludge from a WWTP under methanogenic conditions. Environmental Science & Technology, 47(9): 4227–4235

[56] Zhang Y, Liu J, Moores A, Ghoshal S. (2020). Transformation of 6:2 fluorotelomer sulfonate by cobalt(ii)-activated peroxymonosulfate. Environmental Science & Technology, 54(7): 4631–4640

[57] Zhu C, Bao G, Huang S. (2016). Optimization of laccase production in the white-rot fungus Pleurotus ostreatus (ACCC 52857) induced through yeast extract and copper. Biotechnology, Biotechnological Equipment, 30(2): 270–276

Acknowledgements

The authors acknowledge generous analytical, financial, and technical support by the Center for Air and Aquatic Resources Engineering and Sciences (CAARES) at Clarkson University and thank the employees at the Center of Forest Mycology Research (CFMR) in Madison, WI, for providing all cultures used in this research. The authors also thank E. Dee Brown, MS, and Dr. Sivachandiran Loganathan for assistance with sulfate analysis.

Conflict of Interests

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-024-1867-5 and is accessible for authorized users.

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