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

doi:10.1007/s11783-024-1867-5

Front. Environ. Sci. Eng.

2024, Vol. 18

Issue (9) : 107 https://doi.org/10.1007/s11783-024-1867-5

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

Felix Grimberg, Thomas M Holsen, Sujan Fernando, Siwen Wang(

)

Department of Civil and Environmental Engineering, Clarkson University, Potsdam, New York 13699, USA

Download: PDF(3764 KB) HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks

Abstract

● 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.

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

Corresponding Author(s): Siwen Wang

Issue Date: 13 June 2024

Cite this article:

Felix Grimberg,Thomas M Holsen,Sujan Fernando, et al. Biotransformation of 6:2 fluorotelomer sulfonate (6:2 FTS) in sulfur-rich media by Trametopsis cervina[J]. Front. Environ. Sci. Eng., 2024, 18(9): 107.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-024-1867-5
https://academic.hep.com.cn/fese/EN/Y2024/V18/I9/107

Fig.1 Molar balance of 6:2 FTS with products and PFOA in Control, P. ostreatus, and T. cervina sample groups. Error bars represent standard deviations (n = 3).

Fig.2 Molar factions of 6:2 FTS and transformation products during 6:2 FTS biotransformation in Control, P. ostreatus, and T. cervina sample groups. Error bars represent standard deviations (n = 3).

Fig.3 Proposed 6:2 FTS transformation pathway by T. cervina grown in the sulfur-rich medium based on the transformation products identified in this study.

Fig.4 Molar fraction of 6:2 FTS and transformation products during 6:2 FTS transformation by T. cervina, including estimated headspace concentrations of 5:2 ketone and 5:2 sFTOH. Transient intermediates are on top, stable products are on the bottom, and 6:2 FTS is in the middle. Error bars represent standard deviations of molar recovery of added 6:2 FTS in triplicate samples, including estimated concentrations of headspace analytes, which is the sum standard deviations of 6:2 FTS and transformation product concentrations (in molar percent basis) shown in Fig. 2.

Tab.1 Sulfate concentrations and days until 50% degradation of 6:2 FTS in this study and other aerobic biotransformation studies

Fig.5 Sulfate concentrations during 6:2 FTS transformation in T. cervina group samples.

1	W J Backe, T C Day, J A Field. (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 https://doi.org/10.1021/es3034999
2	K A Barzen-Hanson, S C Roberts, S Choyke, K Oetjen, A McAlees, N Riddell, R McCrindle, P L Ferguson, C P Higgins, J A Field. (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 https://doi.org/10.1021/acs.est.6b05843
3	R C Buck (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	C Cachet, M Keddam, V Mariotte, R Wiart. (1993). Adsorption of perfluorinated surfactants on gold electrodes—II. Behaviour of ionic compounds. Electrochimica Acta, 38(15): 2203–2208 https://doi.org/10.1016/0013-4686(93)80099-L
5	C Cachet, M Keddam, V Mariotte, R Wiart. (1994). Influence of perfluorinated and hydrogenated surfactants upon hydrogen evolution on gold electrodes. Electrochimica Acta, 39(18): 2743–2750 https://doi.org/10.1016/0013-4686(94)E0188-6
6	L P Christopher, B Yao, Y Ji. (2014). Lignin biodegradation with laccase-mediator systems. Frontiers in Energy Research, 2: 12 https://doi.org/10.3389/fenrg.2014.00012
7	D Cui, X Li, N Quinete. (2020). Occurrence, fate, sources and toxicity of PFAS: What we know so far in Florida and major gaps. Trends in Analytical Chemistry, 130: 115976 https://doi.org/10.1016/j.trac.2020.115976
8	L A D’Agostino, S A Mabury. (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 https://doi.org/10.1021/acs.est.7b03994
9	DuPont (2010). DuPont Surface Protection Solutions. DuPontTM Capstone® Repellent and Surfactants Product Stewardship Detail. Wilmington: DuPont Experimental Station
10	J A Field, J Seow. (2017). Properties, occurrence, and fate of fluorotelomer sulfonates. Critical Reviews in Environmental Science and Technology, 47(8): 643–691 https://doi.org/10.1080/10643389.2017.1326276
11	P C I Franco, I S Shiraishi, R F H Dekker, A M Barbosa-Dekker, D Borsato, K B Angilelli, G P C Evaristo, J I Simionato, J F S Daniel (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	H Hamid, L Y Li, J R Grace. (2020a). Formation of perfluorocarboxylic acids from 6:2 fluorotelomer sulfonate (6:2 FTS) in landfill leachate: role of microbial communities. Environmental Pollution, 259: 113835 https://doi.org/10.1016/j.envpol.2019.113835
13	H Hamid, L Y Li, J R Grace. (2020b). Effect of substrate concentrations on aerobic biotransformation of 6:2 fluorotelomer sulfonate (6:2 FTS) in landfill leachate. Chemosphere, 261: 128108 https://doi.org/10.1016/j.chemosphere.2020.128108
14	T Hirano, Y Honda, T Watanabe, M Kuwahara. (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 https://doi.org/10.1271/bbb.64.1958
15	R A Hoke, B D Ferrell, T Ryan, T L Sloman, J W Green, D L Nabb, R Mingoia, R C Buck, S H Korzeniowski. (2015). Aquatic hazard, bioaccumulation and screening risk assessment for 6:2 fluorotelomer sulfonate. Chemosphere, 128: 258–265 https://doi.org/10.1016/j.chemosphere.2015.01.033
16	S G Karp, V Faraco, A Amore, L Birolo, C Giangrande, V T Soccol, A Pandey, C R Soccol. (2012). Characterization of laccase isoforms produced by Pleurotus ostreatus in solid state fermentation of sugarcane bagasse. Bioresource Technology, 114: 735–739 https://doi.org/10.1016/j.biortech.2012.03.058
17	A Kärrman, K Elgh-Dalgren, C Lafossas, T Møskeland. (2011). Environmental levels and distribution of structural isomers of perfluoroalkyl acids after aqueous fire-fighting foam (AFFF) contamination. Environmental Chemistry, 8(4): 372 https://doi.org/10.1071/EN10145
18	S Korzeniowski, T Cortina. (2008) foams Firefighting . S Korzeniowski, R C Buch, D M Kempisty, et al. Ed. Perfluoroalkyl Substances in the Environment. Boca Raton: CRC Press
19	U Kües (2015). Fungal enzymes for environmental management. Current Opinion in Biotechnology, 33, 268–278 10.1016/j.copbio.2015.03.006
20	S Kurwadkar, J Dane, S R Kanel, M N Nadagouda, R W Cawdrey, B Ambade, G C Struckhoff, R Wilkin. (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 https://doi.org/10.1016/j.scitotenv.2021.151003
21	J Liu, N Wang, B Szostek, R C Buck, P K Panciroli, P W Folsom, L M Sulecki, C A Bellin. (2010). Fluorotelomer alcohol aerobic biodegradation in soil and mixed bacterial culture. Chemosphere, 78(4): 437–444 https://doi.org/10.1016/j.chemosphere.2009.10.044
22	M Liu, G Munoz, Duy S Vo, S Sauvé, J Liu. (2022). Per- and polyfluoroalkyl substances in contaminated soil and groundwater at airports: a Canadian case study. Environmental Science & Technology, 56(2): 885–895 https://doi.org/10.1021/acs.est.1c04798
23	Q Luo, S Liang, Q Huang. (2018a). Laccase induced degradation of perfluorooctanoic acid in a soil slurry. Journal of Hazardous Materials, 359: 241–247 https://doi.org/10.1016/j.jhazmat.2018.07.048
24	Q Luo, Z Wang, M Feng, D Chiang, D Woodward, S Liang, J Lu, Q Huang. (2017). Factors controlling the rate of perfluorooctanoic acid degradation in laccase-mediator systems: the impact of metal ions. Environmental Pollution, 224: 649–657 https://doi.org/10.1016/j.envpol.2017.02.050
25	Q Luo, X Yan, J Lu, Q Huang. (2018b). Perfluorooctanesulfonate degrades in a laccase-mediator system. Environmental Science & Technology, 52(18): 10617–10626 https://doi.org/10.1021/acs.est.8b00839
26	V Méndez, S Holland, S Bhardwaj, J McDonald, S Khan, D O’Carroll, R Pickford, S Richards, C O’Farrell, N Coleman. et al.. (2022). Aerobic biotransformation of 6:2 fluorotelomer sulfonate by Dietzia aurantiaca J3 under sulfur-limiting conditions. Science of the Total Environment, 829: 154587 https://doi.org/10.1016/j.scitotenv.2022.154587
27	N Merino, M Wang, R Ambrocio, K Mak, E O’Connor, A Gao, E L Hawley, R A Deeb, L Y Tseng, S Mahendra. (2018). Fungal biotransformation of 6:2 fluorotelomer alcohol. Remediation Journal, 28(2): 59–70 https://doi.org/10.1002/rem.21550
28	M K Moe, S Huber, J Svenson, A Hagenaars, M Pabon, M Trümper, U Berger, D Knapen, D Herzke. (2012). The structure of the fire fighting foam surfactant Forafac®1157 and its biological and photolytic transformation products. Chemosphere, 89(7): 869–875 https://doi.org/10.1016/j.chemosphere.2012.05.012
29	Č Novotný, K Svobodová, P Erbanová, T Cajthaml, A Kasinath, E Lang, V Šašek. (2004). Ligninolytic fungi in bioremediation: extracellular enzyme production and degradation rate. Soil Biology & Biochemistry, 36(10): 1545–1551 https://doi.org/10.1016/j.soilbio.2004.07.019
30	B J Place, J A Field. (2012a). Identification of novel fluorochemicals in aqueous film-forming foams used by the US military. Environmental Science & Technology, 46(13): 7120–7127 https://doi.org/10.1021/es301465n
31	B J Place, J A Field. (2012b). Identification of novel fluorochemicals in aqueous film-forming foams used by the US military. Environmental Science & Technology, 46(13): 7120–7127 https://doi.org/10.1021/es301465n
32	R Riaz, M Junaid, M Y A Rehman, T Iqbal, J A Khan, Y Dong, L Yue, Y Chen, N Xu, R N Malik. (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 https://doi.org/10.1016/j.scitotenv.2022.159144
33	S Ritter. (2010). Fluorochemicals go short. Chem. Eng. News Archive, 88: 12–17 https://doi.org/10.1021/cen-v088n005.p012
34	T Ruan, B Szostek, P W Folsom, B W Wolstenholme, R Liu, J Liu, G Jiang, N Wang, R C Buck. (2013). Aerobic soil biotransformation of 6:2 fluorotelomer iodide. Environmental Science & Technology, 47(20): 11504–11511 https://doi.org/10.1021/es4018128
35	C Ruttkies, E L Schymanski, S Wolf, J Hollender, S Neumann. (2016). MetFrag relaunched: incorporating strategies beyond in silico fragmentation. Journal of Cheminformatics, 8(1): 3 https://doi.org/10.1186/s13321-016-0115-9
36	M M Schultz, D F Barofsky, J A Field. (2004). Quantitative determination of fluorotelomer sulfonates in groundwater by LC MS/MS. Environmental Science & Technology, 38(6): 1828–1835 https://doi.org/10.1021/es035031j
37	T Schwichtenberg, D Bogdan, C C Carignan, P Reardon, J Rewerts, T Wanzek, J A Field. (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 https://doi.org/10.1021/acs.est.0c05697
38	N Shakhova. (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 https://doi.org/10.5943/cream/10/1/12
39	D M J Shaw, G Munoz, E M Bottos, S V Duy, S Sauvé, J Liu, Hamme J D Van. (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 https://doi.org/10.1016/j.scitotenv.2018.08.012
40	Y Shi (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	M Shojaei, N Kumar, S Chaobol, K Wu, M Crimi, J Guelfo. (2021). Enhanced recovery of per- and polyfluoroalkyl substances (PFASs) from impacted soils using heat activated persulfate. Environmental Science & Technology, 55(14): 9805–9816 https://doi.org/10.1021/acs.est.0c08069
42	D Singh, S Chen. (2008). The white-rot fungus Phanerochaete chrysosporium: conditions for the production of lignin-degrading enzymes. Applied Microbiology and Biotechnology, 81(3): 399–417 https://doi.org/10.1007/s00253-008-1706-9
43	A K Sista Kameshwar, W Qin. (2018). Comparative study of genome-wide plant biomass-degrading CAZymes in white rot, brown rot and soft rot fungi. Mycology, 9(2): 93–105 https://doi.org/10.1080/21501203.2017.1419296
44	E M Sunderland, X C Hu, C Dassuncao, A K Tokranov, C C Wagner, J G Allen. (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 https://doi.org/10.1038/s41370-018-0094-1
45	A Tang, X Zhang, R Li, W Tu, H Guo, Y Zhang, Z Li, Y Liu, B Mai. (2022). Spatiotemporal distribution, partitioning behavior and flux of per- and polyfluoroalkyl substances in surface water and sediment from Poyang Lake, China. Chemosphere, 295: 133855 https://doi.org/10.1016/j.chemosphere.2022.133855
46	N Tseng, N Wang, B Szostek, S Mahendra. (2014). Biotransformation of 6:2 fluorotelomer alcohol (6:2 FTOH) by a wood-rotting fungus. Environmental Science & Technology, 48(7): 4012–4020 https://doi.org/10.1021/es4057483
47	P Vaithanomsat, A Sangnam, T Boonpratuang, R Choeyklin, P Promkiam-on, S Chuntranuluck, T Kreetachat. (2013). Wood degradation and optimized laccase production by resupinate white-rot fungi in northern Thailand: bioresources. Bioresource Technology, 8: 6342–6360
48	J D Van Hamme, E M Bottos, N J Bilbey, S E Brewer. (2013). Genomic and proteomic characterization of Gordonia sp. NB4–1Y in relation to 6 : 2 fluorotelomer sulfonate biodegradation. Microbiology, 159(Pt_8): 1618–1628 https://doi.org/10.1099/mic.0.068932-0
49	M Vrsanska, S Voberkova, V Langer, D Palovcikova, A Moulick, V Adam, P Kopel. (2016). Induction of laccase, lignin peroxidase and manganese peroxidase activities in white-rot fungi using copper complexes. Molecules, 21(11): 1553 https://doi.org/10.3390/molecules21111553
50	N Wang, J Liu, R C Buck, S H Korzeniowski, B W Wolstenholme, P W Folsom, L M Sulecki. (2011). 6:2 Fluorotelomer sulfonate aerobic biotransformation in activated sludge of waste water treatment plants. Chemosphere, 82(6): 853–858 https://doi.org/10.1016/j.chemosphere.2010.11.003
51	S Wolf, S Schmidt, M Müller-Hannemann, S Neumann. (2010). In silico fragmentation for computer assisted identification of metabolite mass spectra. BMC Bioinformatics, 11(1): 148 https://doi.org/10.1186/1471-2105-11-148
52	S H Yang, Y Shi, M Strynar, K H Chu. (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 https://doi.org/10.1016/j.jhazmat.2021.127052
53	T Yin, N H Tran, C Huiting, Y He, K Y H Gin. (2019). Biotransformation of polyfluoroalkyl substances by microbial consortia from constructed wetlands under aerobic and anoxic conditions. Chemosphere, 233: 101–109 https://doi.org/10.1016/j.chemosphere.2019.05.227
54	S Zhang, X Lu, N Wang, R Buck. (2016). Biotransformation potential of 6:2 fluorotelomer sulfonate (6:2 FTSA) in aerobic and anaerobic sediment. Chemosphere, 154: 224–230 https://doi.org/10.1016/j.chemosphere.2016.03.062
55	S Zhang, B Szostek, P K McCausland, B W Wolstenholme, X Lu, N Wang, R C Buck. (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 https://doi.org/10.1021/es4000824
56	Y Zhang, J Liu, A Moores, S Ghoshal. (2020). Transformation of 6:2 fluorotelomer sulfonate by cobalt(ii)-activated peroxymonosulfate. Environmental Science & Technology, 54(7): 4631–4640 https://doi.org/10.1021/acs.est.9b07113
57	C Zhu, G Bao, S Huang. (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 https://doi.org/10.1080/13102818.2015.1135081

[1]

FSE-24049-OF-GF_suppl_1

Download

[1]	Yiquan Wu, Ying Xu, Ningyi Zhou. A newly defined dioxygenase system from Mycobacterium vanbaalenii PYR-1 endowed with an enhanced activity of dihydroxylation of high-molecular-weight polyaromatic hydrocarbons[J]. Front. Environ. Sci. Eng., 2020, 14(1): 14-.
[2]	Xiuhua LI, Haibo ZHANG, Yongming LUO, Ying TENG. Remediation of soil heavily polluted with polychlorinated biphenyls using a low-temperature plasma technique[J]. Front Envir Sci Eng, 2014, 8(2): 277-283.
[3]	Tao PAN, Suizhou REN, Jun GUO, Meiying XU, Guoping SUN. Biosorption and biotransformation of crystal violet by Aeromonas hydrophila DN322p[J]. Front Envir Sci Eng, 2013, 7(2): 185-190.
[4]	ZHOU Xiaoyan, WEN Xianghua, FENG Yan. Influence of glucose feeding on the ligninolytic enzyme production of the white-rot fungus Phanerochaete chrysosporium[J]. Front.Environ.Sci.Eng., 2007, 1(1): 89-94.

Viewed

Full text

Abstract

Cited

Shared

Discussed