Impact of Long-Term Perfluorooctanoic Acid (PFOA) Exposure on Activated Sludge Process

  • Xiaolong Yu
  • Fumitake Nishimura
  • Taira Hidaka


Poly- and perfluorinated alkyl substances (PFASs) are groups of persistent toxic substances that have been commonly detected in wastewater treatment plants (WWTPs). In some cases, the activated sludge (AS) in WWTPs will encounter special wastewaters containing PFASs up to tens of milligram per liter (mg L−1). However, under this condition, the potential impacts of PFASs on AS process remain unclear. In the present research, a lab-scale sequencing batch reactor was continuously exposed to perfluorooctanoic acid (PFOA), used as a representation for PFASs, at 20 mg L−1 to mimic the extreme condition. The objective is to explore the impact of PFOA on AS process in terms of its wastewater treatment performance and evolution of microbial communities. The results indicate that PFOA restrained the microbial growth and affected the dissolved organic carbon removal. These negative impacts could be recovered after long-term adaptation. Besides, 20 mg L−1 PFOA shows limited inhibition on nitrification and denitrification, suggesting a safe exposure level of PFOA for nitrogen removal. For microbial evolution, PFOA induced changes of communities during long-term exposure. The high abundance of Bacteroidetes, Proteobacteria, and Acidobacteria maintained over time reveals their tolerance towards PFOA. The occurrences of PFOA-resistant species are also observed. The present research provides new insight into the possible impacts of typical PFAS at high concentrations on AS process.


PFOA Activated sludge Microbial community Wastewater treatment performance 



Xiaolong YU receives the financial support from the China Scholarship Council (CSC, No. 201508050090). Mr. Chisato MATSUMURA and Mr. Ryosuke YOSHIKI in Hyogo Prefectural Institute of Environmental Sciences are appreciated for their cooperation of collecting inoculum sludge. This study was supported by the GAIA Project (Gesuido Academic Incubation to Advanced Project, 2015) of Japanese Ministry of Land, Infrastructure, Transport and Tourism. This study was also supported by Charitable Trust Sewage Works Promotion Fund (No. 28-16), Japan Sewage Works Association.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interest.

Supplementary material

11270_2018_3760_MOESM1_ESM.pdf (1.2 mb)
ESM 1 (PDF 1.18 mb)


  1. Ahrens, L. (2011). Polyfluoroalkyl compounds in the aquatic environment: A review of their occurrence and fate. Journal of Environmental Monitoring, 13(1), 20–31. Scholar
  2. Aquino, S. F., & Stuckey, D. C. (2004). Soluble microbial products formation in anaerobic chemostats in the presence of toxic compounds. Water Research, 38(2), 255–266. Scholar
  3. Barns, S. M., Cain, E. C., Sommerville, L., & Kuske, C. R. (2007). Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Applied and Environmental Microbiology, 73(9), 3113–3116. Scholar
  4. Convention, S. (2015). Proposal to list pentadecafluorooctanoic acid (CAS No: 335-67-1, PFOA, perfluorooctanoic acid), its salts and PFOA-related compounds in Annexes A, B and/or C to the Stockholm Convention on Persistent Organic Pollutants.Google Scholar
  5. Dassuncao, C., Hu, X. C., Zhang, X., Bossi, R., Dam, M., Mikkelsen, B., & Sunderland, E. M. (2017). Temporal shifts in poly- and perfluoroalkyl substances (PFASs) in North Atlantic pilot whales indicate large contribution of atmospheric precursors. Environmental Science and Technology, 51(8), 4512–4521. Scholar
  6. Du, Z., Deng, S., Bei, Y., Huang, Q., Wang, B., Huang, J., & Yu, G. (2014). Adsorption behavior and mechanism of perfluorinated compounds on various adsorbents—A review. Journal of Hazardous Materials.
  7. Han, J. C., Liu, Y., Liu, X., Zhang, Y., Yan, Y. W., Dai, R. H., et al. (2013). The effect of continuous Zn (II) exposure on the organic degradation capability and soluble microbial products (SMP) of activated sludge. Journal of Hazardous Materials, 244–245, 489–494. Scholar
  8. Hekster, F. M., Laane, R. W. P. M., & de Voogt, P. (2003). Environmental and toxicity effects of perfluoroalkylated substances. Reviews of Environmental Contamination and Toxicology, 179, 99–121. Scholar
  9. Hill, T. C. J., Walsh, K. A., Harris, J. A., & Moffett, B. F. (2003). Using ecological diversity measures with bacterial communities. FEMS Microbiology Ecology, 43(1), 1–11. Scholar
  10. Hori, H., Yamamoto, A., Hayakawa, E., Taniyasu, S., Yamashita, N., Kutsuna, S., et al. (2005). Efficient decomposition of environmentally persistent perfluorocarboxylic acids by use of persulfate as a photochemical oxidant. Environmental Science & Technology, 39(7), 2383–2388. Scholar
  11. Houtz, E. F., Sutton, R., Park, J. S., & Sedlak, M. (2016). Poly- and perfluoroalkyl substances in wastewater: Significance of unknown precursors, manufacturing shifts, and likely AFFF impacts. Water Research, 95, 142–149. Scholar
  12. Hughes, J. B., Hellmann, J. J., Ricketts, T. H., & Bohannan, B. J. M. (2001). Counting the uncountable: statistical approaches to estimating microbial diversity. Applied and Environmental Microbiology. doi:
  13. Hunter, P. R., & Gaston, M. A. (1988). Numerical index of the discriminatory ability of typing systems: An application of Simpson’s index of diversity. Journal of Clinical Microbiology, 26(11), 2465–2466 doi:0095-1137/88/112465-02$02.00/0.Google Scholar
  14. Japan Sewage Works Association. (2012). Japanese standard methods for sewage test. Japan: Tokyo.Google Scholar
  15. KEMI Swedish Chemical Agency. (2015). Occurrence and use of highly fluorinated substances and alternatives. Report.Google Scholar
  16. Kong, Q., He, X., Ma, S., Feng, Y., Miao, M., Du, Y., et al. (2017). The performance and evolution of bacterial community of activated sludge exposed to trimethoprim in a sequencing batch reactor. Bioresource Technology.
  17. Lau, C., Anitole, K., Hodes, C., Lai, D., Pfahles-Hutchens, A., & Seed, J. (2007). Perfluoroalkyl acids: A review of monitoring and toxicological findings. Toxicological Sciences.
  18. Lau, C., Butenhoff, J. L., & Rogers, J. M. (2004). The developmental toxicity of perfluoroalkyl acids and their derivatives. Toxicology and Applied Pharmacology.
  19. Lee, J. W., Lee, J. W., Shin, Y. J., Kim, J. E., Ryu, T. K., Ryu, J., et al. (2017). Multi-generational xenoestrogenic effects of Perfluoroalkyl acids (PFAAs) mixture on Oryzias latipes using a flow-through exposure system. Chemosphere, 169, 212–223. Scholar
  20. Li, J., Liu, X., Liu, Y., Ramsay, J., Yao, C., & Dai, R. (2011). The effect of continuous exposure of copper on the properties and extracellular polymeric substances (EPS) of bulking activated sludge. Environmental Science and Pollution Research, 18(9), 1567–1573. Scholar
  21. Li, L., Wang, T., Sun, Y., Wang, P., Yvette, B., Meng, J., et al. (2017). Identify biosorption effects of Thiobacillus towards perfluorooctanoic acid (PFOA): Pilot study from field to laboratory. Chemosphere, 171, 31–39. Scholar
  22. Lin, A. Y.-C., Panchangam, S. C., & Lo, C.-C. (2009). The impact of semiconductor, electronics and optoelectronic industries on downstream perfluorinated chemical contamination in Taiwanese rivers. Environmental Pollution, 157(4), 1365–1372. Scholar
  23. Lindstrom, A. B., Strynar, M. J., & Libelo, E. L. (2011). Polyfluorinated compounds: Past, present, and future. Environmental Science and Technology, 45(19), 7954–7961. Scholar
  24. Liou, J. S.-C., Szostek, B., DeRito, C. M., & Madsen, E. L. (2010). Investigating the biodegradability of perfluorooctanoic acid. Chemosphere, 80(2), 176–183. Scholar
  25. Liu, G., Zhang, S., Yang, K., Zhu, L., & Lin, D. (2016). Toxicity of perfluorooctane sulfonate and perfluorooctanoic acid to Escherichia coli: Membrane disruption, oxidative stress, and DNA damage induced cell inactivation and/or death. Environmental pollution (Barking, Essex : 1987), 214, 806–815. Scholar
  26. Moody, C. A., & Field, J. A. (1999). Determination of perfluorocarboxylates in groundwater impacted by fire-fighting activity determination of perfluorocarboxylates in groundwater impacted by fire-fighting activity. Environmental Science and Technology, 33(16), 2800–2806. Scholar
  27. Niu, J., Li, Y., Shang, E., Xu, Z., & Liu, J. (2016). Electrochemical oxidation of perfluorinated compounds in water. Chemosphere, 146, 526–538. Scholar
  28. Ochoa-Herrera, V., Field, J. A., Luna-Velasco, A., & Sierra-Alvarez, R. (2016). Microbial toxicity and biodegradability of perfluorooctane sulfonate (PFOS) and shorter chain perfluoroalkyl and polyfluoroalkyl substances (PFASs). Environmental Science Processes & Impactts, 18, 1236–1246. Scholar
  29. Park, J. Y., & Yoo, Y. J. (2009). Biological nitrate removal in industrial wastewater treatment: Which electron donor we can choose. Applied Microbiology and Biotechnology.
  30. Parsons, J. R., Sáez, M., Dolfing, J., & de Voogt, P. (2008). Biodegradation of perfluorinated compounds. Reviews of Environmental Contamination and Toxicology, 196, 53–71. Scholar
  31. Prevedouros, K., Cousins, I. T., Buck, R. C., & Korzeniowski, S. H. (2006). Sources, fate and transport of perfluorocarboxylates. Environmental Science and Technology.
  32. Qiu, G., Wirianto, K., Sun, Y., & Ting, Y. (2016). Effect of silver nanoparticles on system performance and microbial community dynamics in a sequencing batch reactor. Journal of Cleaner Production, 130, 137–142. Scholar
  33. Rittmann, B. E., & McCarty, P. L. (2001). Environmental biotechnology: Principles and applications. Biotechnology.
  34. Rodea-Palomares, I., Makowski, M., Gonzalo, S., González-Pleiter, M., Leganés, F., & Fernández-Piñas, F. (2015). Effect of PFOA/PFOS pre-exposure on the toxicity of the herbicides 2,4-D, Atrazine, Diuron and Paraquat to a model aquatic photosynthetic microorganism. Chemosphere, 139, 65–72. Scholar
  35. 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. Scholar
  36. Singleton, D. R., Furlong, M. A., Rathbun, S. L., & Whitman, W. B. (2001). Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Applied and Environmental Microbiology, 67(9), 4374–4376. Scholar
  37. Steinle-Darling, E., & Reinhard, M. (2008). Nanofiltration for trace organic contaminant removal: Structure, solution, and membrane fouling effects on the rejection of perfluorochemicals. Environmental Science and Technology, 42(14), 5292–5297. Scholar
  38. Stockholm Convention. (2009). Stockholm convention on persistent organic pollutants (POPs). In Stockholm Convention on Persistent Organic Pollutants (POPs) (p. 64).Google Scholar
  39. Stratton, G. R., Dai, F., Bellona, C. L., Holsen, T. M., Dickenson, E. R. V., & Mededovic Thagard, S. (2017). Plasma-based water treatment: Efficient transformation of perfluoroalkyl substances (PFASs) in prepared solutions and contaminated groundwater. Environmental Science & Technology, acs.Est.6b04215. doi:
  40. Sun, Y., Wang, T., Peng, X., Wang, P., & Lu, Y. (2016). Bacterial community compositions in sediment polluted by perfluoroalkyl acids (PFAAs) using Illumina high-throughput sequencing. Environmental Science and Pollution Research International, 23(11), 10556–10565. Scholar
  41. Wang, Z., Cousins, I. T., Scheringer, M., Buck, R. C., & Hungerbühler, K. (2014). Global emission inventories for C4-C14 perfluoroalkyl carboxylic acid (PFCA) homologues from 1951 to 2030, part I: production and emissions from quantifiable sources. Environment International.
  42. Wang, Z., DeWitt, J. C., Higgins, C. P., & Cousins, I. T. (2017). A never-ending story of per- and polyfluoroalkyl substances (PFASs)? Environmental Science & Technology, acs.Est.6b04806. doi:
  43. Ward, N. L., Challacombe, J. F., Janssen, P. H., Henrissat, B., Coutinho, P. M., Wu, M., et al. (2009). Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Applied and Environmental Microbiology, 75(7), 2046–2056. Scholar
  44. Weathers, T. S., Harding-Marjanovic, K., Higgins, C. P., Alvarez-Cohen, L., & Sharp, J. O. (2016). Perfluoroalkyl acids inhibit reductive dechlorination of trichloroethene by repressing dehalococcoides. Environmental Science and Technology, 50(1), 240–248. Scholar
  45. Weathers, T. S., Higgins, C. P., & Sharp, J. O. (2015). Enhanced biofilm production by a toluene-degrading rhodococcus observed after exposure to perfluoroalkyl acids. Environmental Science and Technology, 49(9), 5458–5466. Scholar
  46. Wu, W., Duan, T., Song, H., Li, Y., Yu, A., Zhang, L., & Li, A. (2015). The effect of continuous Ni(II) exposure on the organic degradation and soluble microbial product (SMP) formation in two-phase anaerobic reactor. Journal of Environmental Sciences (China), 33, 78–87. Scholar
  47. Xiao, F., Halbach, T. R., Simcik, M. F., & Gulliver, J. S. (2012). Input characterization of perfluoroalkyl substances in wastewater treatment plants: Source discrimination by exploratory data analysis. Water Research, 46(9), 3101–3109. Scholar
  48. Yang, M., Ye, J., Qin, H., Long, Y., & Li, Y. (2016). Influence of perfluorooctanoic acid on proteomic expression and cell membrane fatty acid of Escherichia coli. Environmental Pollution, 220, 532–539. Scholar
  49. Yang, Y., Lv, Q. Y., Guo, L. H., Wan, B., Ren, X. M., Shi, Y. L., & Cai, Y. Q. (2017). Identification of protein tyrosine phosphatase SHP-2 as a new target of perfluoroalkyl acids in HepG2 cells. Archives of Toxicology, 91(4), 1697–1707. Scholar
  50. Yang, Y., Quensen, J., Mathieu, J., Wang, Q., Wang, J., Li, M., et al. (2014). Pyrosequencing reveals higher impact of silver nanoparticles than Ag+ on the microbial community structure of activated sludge. Water Research, 48(1), 317–325. Scholar
  51. You, J., Das, A., Dolan, E. M., & Hu, Z. (2009). Ammonia-oxidizing archaea involved in nitrogen removal. Water Research.
  52. Yu, J., Hu, J., Tanaka, S., & Fujii, S. (2009). Perfluorooctane sulfonate (PFOS) and perfluorooctanoic acid (PFOA) in sewage treatment plants. Water Research, 43(9), 2399–2408. Scholar
  53. Yu, X., Nishimura, F., & Hidaka, T. (2018). Effects of microbial activity on perfluorinated carboxylic acids (PFCAs) generation during aerobic biotransformation of fluorotelomer alcohols in activated sludge. Science of the Total Environment, 610–611, 776–785. Scholar
  54. Yu, X., Takabe, Y., Yamamoto, K., Matsumura, C., & Nishimura, F. (2016). Biodegradation property of 8:2 fluorotelomer alcohol (8:2 FTOH) under aerobic/anoxic/anaerobic conditions. Journal of Water and Environment Technology, 14(3), 177–190. Scholar
  55. Zareitalabad, P., Siemens, J., Hamer, M., & Amelung, W. (2013). Perfluorooctanoic acid (PFOA) and perfluorooctanesulfonic acid (PFOS) in surface waters, sediments, soils and wastewater—A review on concentrations and distribution coefficients. Chemosphere.
  56. Zhang, S., Merino, N., Wang, N., Ruan, T., & Lu, X. (2016). Impact of 6:2 fluorotelomer alcohol aerobic biotransformation on a sediment microbial community. The Science of the total environment. doi:

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Environmental Engineering, Graduate School of EngineeringKyoto UniversityKyotoJapan

Personalised recommendations