Environmental Science and Pollution Research

, Volume 25, Issue 10, pp 9342–9350 | Cite as

The acute effects of erythromycin and oxytetracycline on enhanced biological phosphorus removal system: shift in bacterial community structure

  • Zhetai Hu
  • Peide Sun
  • Jingyi Han
  • Ruyi Wang
  • Liang Jiao
  • Pengfei Yang
  • Jing Cai
Research Article


Since extensive application, an increasing amount of antibiotics has been released into wastewater treatment plants. In this study, the enhanced biological phosphorus removal (EBPR) system was fed with synthetic wastewater containing erythromycin (ERY) and oxytetracycline (OTC) for 7 days to evaluate the variations of solution ortho-P (SOP), volatile fatty acid (VFA), poly-bhydroxyalkanoates (PHAs), specific oxygen uptake rater (SOUR), and microbial community in the EBPR system. The obtained results showed that the P-removal efficiency decreased to 0.0%, and at the end of the experiment, only less than 20% of the VFA could be consumed. Besides, the variable processes of P and PHAs were destroyed. Moreover, to better grasp the inhibitory mechanism of antibiotics, microbial community compositions of activated sludge sampled in all reactors were investigated by high-throughput sequencing techniques. Results of comparative and evolutionary analysis revealed that high concentrations (5 and 10 mg/L) of ERY and OTC could seriously shift microbial communities, while combined antibiotics could induce more. Additionally, Accumulibacter and Competibacter were two primary microorganisms at the genus level in the EBPR system. Accumulibacter decreased seriously for exposure to antibiotics, while Competibacter increased in all experimental reactors especially in combined antibiotics reactor.


Enhanced biological phosphorus removal Erythromycin Oxytetracycline Combined antibiotics effect Microbial community composition 


Funding information

The study was financially supported by the National Natural Science Foundation of China (No. 21606196), Major Scientific and Technological Project of Zhejiang Province (No. 2014C03002), Scientific Research Fund of Zhejiang Provincial Education Department (No. Y201635678), and Scientific Research Fund of Zhejiang Provincial Education Department (No. Y201635678).

Supplementary material

11356_2018_1221_MOESM1_ESM.docx (1.2 mb)
ESM 1 (DOCX 1212 kb)


  1. Alighardashi A, Pandolfi D, Potier O, Pons MN (2009) Acute sensitivity of activated sludge bacteria to erythromycin. J. Hazard Mater 172(2–3):685–692. CrossRefGoogle Scholar
  2. Álvarez JA, Otero L, Lema JM, Omil F (2010) The effect and fate of antibiotics during the anaerobic digestion of pig manure. Bioresour Technol 101(22):8581–8586. CrossRefGoogle Scholar
  3. APHA (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, American Water Works Association, Water Pollution Control Federation, Washington, DCGoogle Scholar
  4. Carvalheira M, Oehmen A, Carvalho G, Reis MAM (2014) Survival strategies of polyphosphate accumulating organisms and glycogen accumulating organisms under conditions of low organic loading. Bioresour Technol 172:290–296. CrossRefGoogle Scholar
  5. Chen Y, Chen H, Zheng X, Mu H (2012) The impacts of silver nanoparticles and silver ions on wastewater biological phosphorous removal and the mechanisms. J Hazard Mater 239-240:88–94Google Scholar
  6. Davids M, Gudra D, Radovica-Spalvina I, Fridmanis D, Bartkevics V, Muter O (2017) The effects of ibuprofen on activated sludge: shift in bacterial community structure and resistance to ciprofloxacin. J Hazard Mater 340:291–299. CrossRefGoogle Scholar
  7. Fan C, He ZJ (2011) Proliferation of antibiotic resistance genes in microbial consortia of sequencing batch reactors (SBRs) upon exposure to trace erythromycin or erythromycin-H2O. Water Res 45(10):3098–3106. CrossRefGoogle Scholar
  8. Fatta-Kassinos D, Meric S, Nikolaou A (2011) Pharmaceutical residues in environmental waters and wastewater: current state of knowledge and future research. Anal Bioanal Chem 399(1):251–275. CrossRefGoogle Scholar
  9. Henriques IDS, Love NG (2007) The role of extracellular polymeric substances in the toxicity response of activated sludge bacteria to chemical toxins. Water Res 41(18):4177–4185. CrossRefGoogle Scholar
  10. Hu ZT, Sun PD, Hu ZR, Han JY, Wang RY, Jiao L, Yang PF (2016) Short-term performance of enhanced biological phosphorus removal (EBPR) system exposed to erythromycin (ERY) and oxytetracycline (OTC). Bioresour Technol 221:15–25. CrossRefGoogle Scholar
  11. Hu ZT, Lu XY, Sun PD, Hu ZR, Wang RY, Lou CK, Han JY (2017) Understanding the performance of microbial community induced by ZnO nanoparticles in enhanced biological phosphorus removal system and its recoverability. Bioresour Technol 225:279–285. CrossRefGoogle Scholar
  12. Kong Q, He X, Feng Y, Miao MS, Wang Q, Du YD, Xu F (2017) Pollutant removal and microorganism evolution of activated sludge under ofloxacin selection pressure. Bioresour Technol 241:849–856. CrossRefGoogle Scholar
  13. Kummerer K (2009) The presence of pharmaceuticals in the environment due to human use—present knowledge and future challenges. J Environ Manag 90(8):2354–2366. CrossRefGoogle Scholar
  14. Larsson DGJ, De Pedro C, Paxeus N (2007) Effluent from drug manufactures contains extremely high levels of pharmaceuticals. J. Hazard Mater 148(3):751–755. CrossRefGoogle Scholar
  15. Li B, Zhang T (2010) Biodegradation and adsorption of antibiotics in the activated sludge process. Environ Sci Technol 44(9):3468–3473. CrossRefGoogle Scholar
  16. Li D, Yang M, Hu J, Ren L, Zhang Y, Chang H, Li K (2008a) Determination and fate of oxytetracycline and related compounds in oxytetracycline production wastewater and the receiving river. Environ Toxicol Chem 27(1):80–86. CrossRefGoogle Scholar
  17. Li K, Yediler A, Yang M, Schulte-Hostede S, Wong MH (2008b) Ozonation of oxytetracycline and toxicological assessment of its oxidation by-products. Chemosphere 72(3):473–478. CrossRefGoogle Scholar
  18. Liu H, Yang YK, Ge YH, Zhao L, Long S, Zhang RC (2016) Interaction between common antibiotics and a Shewanella strain isolated from an enhanced biological phosphorus removal activated sludge system. Bioresour Technol 222:114–122. CrossRefGoogle Scholar
  19. Louvet JN, Giammarino C, Potier O, Pons MN (2010) Adverse effects of erythromycin on the structure and chemistry of activated sludge. Environ Pollut 158(3):688–693. CrossRefGoogle Scholar
  20. Lv XM, Shao MF, Li CL, Li J, Gao XL, Sun FY (2013) A comparative study of the bacterial community in denitrifying and traditional enhanced biological phosphorus removal processes. Microbes Environ 29(4):261–268Google Scholar
  21. Motlagh AM, Bhattacharjee AS, Goel R (2015) Microbiological study of bacteriophage induction in the presence of chemical stress factors in enhanced biological phosphorus removal (EBPR). Water Res 81:1–14. CrossRefGoogle Scholar
  22. Noophan P, Narinhongtong P, Wantawin C, Munakata-Marr J (2012) Effects of oxytetracycline on anammox activity. J Environ Sci Health A 47(6):873–877. CrossRefGoogle Scholar
  23. Oehmen A, Keller-Lehmann B, Zeng RJ, Yuan Z, Keller J (2005) Optimisation of poly-b-hydroxyalkanoate analysis using gas chromatography for enhanced biological phosphorus removal systems. J Chromatogr A 1070(1–2):131–136. CrossRefGoogle Scholar
  24. Oehmen A, Lemos PC, Carvalho G, Yuan ZG, Keller J, Blackall LL, Reis MA (2007) Advances in enhanced biological phosphorus removal: from micro to macro scale. Water Res 41(11):2271–2300. CrossRefGoogle Scholar
  25. Ozbayram EG, Arikan O, Ince B, Cetecioglu Z, Aydin S, Ince O (2015) Acute effects of various antibiotic combinations on acetoclastic methanogenic activity. Environmental Science and Pollution Research 22(8):6230–6235Google Scholar
  26. Pala-Ozkok I, Rehman A, Ubay-Cokgor E (2014) Pyrosequencing reveals the inhibitory impact of chronic exposure to erythromycin on activated sludge bacterial community structure. Biochem Eng J 90(90):195–205. CrossRefGoogle Scholar
  27. Smolders G, Van der Meij J, Van Loosdrecht M, Heijnen J (1994) Model of the anaerobic metabolism of the biological phosphorus removal process: stoichiometry and pH influence. Biotechnol Bioeng 44(7):461–470CrossRefGoogle Scholar
  28. Sukul P, Spiteller M (2007) Fluoroquinolone antibiotics in the environment. Rev Environ Contam Toxicol 191:131–162Google Scholar
  29. Tayà C, Garlapati VK, Guisasola A, Baeza JA (2013) The selective role of nitrite in the PAO/GAO competition. Chemosphere 93(4):612–618. CrossRefGoogle Scholar
  30. Vandewalle JL, Goetz GW, Huse SM, Morrison HG, Sogin ML, Hoffmann RG, Yan K, McLellan SL (2012) Acinetobacter, Aeromonas, and Trichococcus populations dominate the microbial community within urban sewer infrastructure. Environ Microbiol 14(9):2538–2552. CrossRefGoogle Scholar
  31. Wang DB, Yang GJ, Li XM, Zheng W, Wu Y, Yang Q, Zeng GM (2012a) Inducing mechanism of biological phosphorus removal driven by the aerobic/extended-idle regime. Biotechnol Bioeng 109(11):2798–2807. CrossRefGoogle Scholar
  32. Wang DB, Li XM, Yang Q, Zeng W, Wu Y, Zeng TJ, Zeng GM (2012b) Improved biological phosphorus removal performance driven by the aerobic/extended-idle regime with propionate as the sole carbon source. Water Res 46(12):3868–3878. CrossRefGoogle Scholar
  33. Wang YL, Wang DB, Liu YW, Wang QL, Chen F, Yang Q, Li XM, Zeng GM, Li H (2017) Triclocarban enhances short-chain fatty acids production from anaerobic fermentation of waste activated sludge. Water Res 127(10):150–161. CrossRefGoogle Scholar
  34. Yang GF, Zhang QQ, Jin RC (2013) Changes in the nitrogen removal performance and the properties of granular sludge in an anammox system under oxytetracycline (OTC) stress. Bioresour Technol 129(129C):65–71. CrossRefGoogle Scholar
  35. Ye L, Pijuan M, Yuan ZG (2010) The effect of free nitrous acid on the anabolic and catabolic processes of glycogen accumulating organisms. Water Res 44(9):2901–2909. CrossRefGoogle Scholar
  36. Yi KX, Wang DB, Yang Q, Li XM, Chen HB, Sun J, An HX, Wang LQ, Deng YC, Liu J, Zeng GM (2017a) Effect of ciprofloxacin on biological nitrogen and phosphorus removal from wastewater. Sci Total Environ 605-606:368–375. CrossRefGoogle Scholar
  37. Yi KX, Wang DB, Yang Q, Li XM, Chen HB, Sun J, An HX, Wang LQ, Deng YC, Liu J, Zeng GM (2017b) Effect of ciprofloxacin on biological nitrogen and phosphorus removal from wastewater. Sci Total Environ 605-606:368–375. CrossRefGoogle Scholar
  38. Zhang YY, Geng JJ, Ma HJ, Ren HQ, Xu K, Ding LL (2016) Characterization of microbial community and antibiotic resistance genes in activated sludge under tetracycline and sulfamethoxazole selection pressure. Sci Total Environ 571:479–486. CrossRefGoogle Scholar
  39. Zheng XL, Sun PD, Lou JQ, Fang ZG, Guo MX, Song YQ, Tang XD, Jiang T (2013) The long-term effect of nitrite on the granule-based enhanced biological phosphorus removal system and the reversibility. Bioresour Technol 132:333–341. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Zhetai Hu
    • 1
  • Peide Sun
    • 1
  • Jingyi Han
    • 1
  • Ruyi Wang
    • 1
  • Liang Jiao
    • 1
  • Pengfei Yang
    • 1
  • Jing Cai
    • 1
  1. 1.School of Environmental Science and EngineeringZhejiang Gongshang UniversityHangzhouChina

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