Environmental Science and Pollution Research

, Volume 22, Issue 6, pp 4587–4596 | Cite as

Antibiotic-resistant genes and antibiotic-resistant bacteria in the effluent of urban residential areas, hospitals, and a municipal wastewater treatment plant system

  • Jianan Li
  • Weixiao Cheng
  • Like Xu
  • P. J. Strong
  • Hong ChenEmail author
Research Article


In this study, we determined the abundance of 8 antibiotics (3 tetracyclines, 4 sulfonamides, and 1 trimethoprim), 12 antibiotic-resistant genes (10 tet, 2 sul), 4 antibiotic-resistant bacteria (tetracycline, sulfamethoxazole, and combined resistance), and class 1 integron integrase gene (intI1) in the effluent of residential areas, hospitals, and municipal wastewater treatment plant (WWTP) systems. The concentrations of total/individual targets (antibiotics, genes, and bacteria) varied remarkably among different samples, but the hospital samples generally had a lower abundance than the residential area samples. The WWTP demonstrated removal efficiencies of 50.8 % tetracyclines, 66.8 % sulfonamides, 0.5 logs to 2.5 logs tet genes, and less than 1 log of sul and intI1 genes, as well as 0.5 log to 1 log removal for target bacteria. Except for the total tetracycline concentration and the proportion of tetracycline-resistant bacteria (R 2 = 0.330, P < 0.05), there was no significant correlation between antibiotics and the corresponding resistant bacteria (P > 0.05). In contrast, various relationships were identified between antibiotics and antibiotic resistance genes (P < 0.05). Tet (A) and tet (B) displayed noticeable relationships with both tetracycline and combined antibiotic-resistant bacteria (P < 0.01).


Antibiotic resistance genes Antibiotic-resistant bacteria Wastewater treatment plant Residential areas Hospitals 



The authors are grateful to the managers of hospitals/residential areas and wastewater treatment plant for providing the samples and information required for this study. Support from the Natural Science Foundation of China (21277117 and 21210008) is gratefully acknowledged.

Supplementary material

11356_2014_3665_MOESM1_ESM.doc (1.7 mb)
ESM 1 (DOC 1,753 kb)


  1. Akinbowale OL, Peng H, Barton MD (2007) Diversity of tetracycline resistance genes in bacteria from aquaculture sources in Australia. J Appl Microbiol 103(5):2016–2025CrossRefGoogle Scholar
  2. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J (2010) Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8:251–259CrossRefGoogle Scholar
  3. Auerbach EA, Seyfried EE, McMahon KD (2007) Tetracycline resistance genes in activated sludge wastewater treatment plants. Water Res 41(5):1143–1151CrossRefGoogle Scholar
  4. Baquero F, Martínez J, Cantón R (2008) Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 19:260–265CrossRefGoogle Scholar
  5. Brooks JP, Maxwell SL, Rensing C, Gerba CP, Pepper IL (2007) Occurrence of antibiotic resistant bacteria and endotoxin associated with the land application of biosolids. Can J Microbiol 53:616–622CrossRefGoogle Scholar
  6. Brown KD, Kulis J, Thomson B, Chapman TH, Mawhinney DB (2006) Occurrence of antibiotics in hospital, residential, and dairy effluent, municipal wastewater, and the Rio Grande in New Mexico. Sci Total Environ 366(2–3):772–783CrossRefGoogle Scholar
  7. Chen H, Zhang M (2013) Occurrence and removal of antibiotic resistance genes in municipal wastewater and rural domestic sewage treatment systems in eastern China. Environ Int 55:9–14CrossRefGoogle Scholar
  8. Cheng WX, Chen H, Su C, Yan SH (2013) Abundance and persistence of antibiotic resistance genes in livestock farms: a comprehensive investigation in eastern China. Environ Int 61:1–7CrossRefGoogle Scholar
  9. Chopra I, Roberts M (2001) Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65(2):232–260CrossRefGoogle Scholar
  10. Davison J (1999) Genetic exchange between bacteria in the environment. Plasmid 42(2):73–91CrossRefGoogle Scholar
  11. Ding Y, Zhang W, Gu C, Xagoraraki I, Li H (2011) Determination of pharmaceuticals in biosolids using accelerated solvent extraction and liquid chromatography/tandem mass spectrometry. J Chromatogr A 1218:10–16CrossRefGoogle Scholar
  12. Gao P, Munir M, Xagoraraki I (2012a) Correlation of tetracycline and sulfonamide antibiotics with corresponding resistance genes and resistant bacteria in a conventional municipal wastewater treatment plant. Sci Total Environ 421–422:173–183CrossRefGoogle Scholar
  13. Gao PP, Mao DQ, Luo Y, Wang LM, Xu BJ, Xu L (2012b) Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Res 46(7):2355–2364CrossRefGoogle Scholar
  14. Huerta B, Marti E, Gros M, López P, Pompêo M, Armengol J, Barceló D, Balcázar JL, Rodríguez-Mozaz S, Marcé R (2013) Exploring the links between antibiotic occurrence, antibiotic resistance, and bacterial communities in water supply reservoirs. Sci Total Environ 456–457:161–170CrossRefGoogle Scholar
  15. Iwane T, Urase T, Yamamoto K (2001) Possible impact of treated wastewater discharge on incidence of antibiotic resistant bacteria in river water. Water Sci Technol 43:91–99Google Scholar
  16. Jiang L, Hu XL, Xu T, Zhang HC, Sheng D, Yin DQ (2013) Prevalence of antibiotic resistance genes and their relationship with antibiotics in the Huangpu River and the drinking water sources, Shanghai, China. Sci Total Environ 458–460:267–272CrossRefGoogle Scholar
  17. Kim SR, Nonaka L, Suzuki S (2004) Occurrence of tetracycline resistance genes tet (M) and tet (S) in bacteria from marine aquaculture sites. FEMS Microbiol Lett 237(1):147–156CrossRefGoogle Scholar
  18. Kim S, Eichhorn P, Jensen JN, Weber AS, Aga DS (2005) Removal of antibiotics in wastewater: effect of hydraulic and solid retention times on the fate of tetracycline in the activated sludge process. Environ Sci Technol 39:5816–5823CrossRefGoogle Scholar
  19. Lamshoft M, Sukul P, Zuhlke S, Spiteller M (2007) Metabolism of 14C-labelled and non-labelled sulfadiazine after administration to pigs. Anal Bioanal Chem 388(8):1733–1745CrossRefGoogle Scholar
  20. Lindberg R, Jarnheimer PA, Olsen B, Johansson M, Tysklind M (2004) Determination of antibiotic substances in hospital sewage water using solid phase extraction and liquid chromatography/mass spectrometry and group analogue internal standards. Chemosphere 57(10):1479–1488CrossRefGoogle Scholar
  21. Livermore D (2004) Can better prescribing turn the tide of resistance? Nat Rev Microbiol 2:73–78CrossRefGoogle Scholar
  22. Luna VA, Roberts MC (1998) The presence of the tetO gene in a variety of tetracycline-resistant Streptococcus pneumoniae serotypes from Washington State. J Antimicrob Chemoth 42:613–619CrossRefGoogle Scholar
  23. Martinez JL (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157:2893–2902CrossRefGoogle Scholar
  24. Mazel D (2006) Integrons: agents of bacterial evolution. Nat Rev Microbiol 4(8):608–620CrossRefGoogle Scholar
  25. McKinney CW, Loftin KA, Meyer MT, Davis JG, Pruden A (2010) Tet and sul antibiotic resistance genes in livestock lagoon of various operation type, configuration, and antibiotic occurrence. Environ Sci Technol 44:6102–6109CrossRefGoogle Scholar
  26. Mispagel H, Gray JT (2005) Antibiotic resistance from wastewater oxidation ponds. Water Environ Res 77(7):2996–3002CrossRefGoogle Scholar
  27. Mokracka J, Koczura R, Kaznowski A (2012) Multiresistant Enterobacteriaceae with class 1 and class 2 integrons in a municipal wastewater treatment plant. Water Res 46:3353–3363CrossRefGoogle Scholar
  28. Nõlvak H, Truu M, Tiirik K, Kr O, Sildvee T, Kaasik A, ManderÜ TJ (2013) Dynamics of antibiotic resistance genes and their relationships with system treatment efficiency in a horizontal subsurface flow constructed wetland. Sci Total Environ 461–462:636–644CrossRefGoogle Scholar
  29. Novo A, Manaia CM (2010) Factors influencing antibiotic resistance burden in municipal wastewater treatment plants. Appl Microbiol Biot 87:1157–1166CrossRefGoogle Scholar
  30. Oberlé K, Capdeville M, Berthe T, Budzinski H, Petit F (2012) Evidence for a complex relationship between antibiotics and antibiotic-resistant Escherichia coli: from medical center patients to a receiving environment. Environ Sci Technol 46:1859–1868CrossRefGoogle Scholar
  31. Peak N, Knapp CW, Yang RK, Hanfelt MM, Smith MS, Aga DS, Graham DW (2007) Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environ Microbiol 9(1):143–151CrossRefGoogle Scholar
  32. Pei R, Kim SC, Carlson KH, Pruden A (2006) Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res 40(12):2427–2435CrossRefGoogle Scholar
  33. Roberts MC (2005) Update on acquired tetracycline resistance genes. FEMS Microbiol Lett 245(2):195–203CrossRefGoogle Scholar
  34. Schwartz T, Kohnen W, Jansen B, Obst U (2003) Detection of antibiotic-resistant bacteria and their resistance genes in waste-water, surface water, and drinking water biofilms. FEMS Microbiol Ecol 43:325–335CrossRefGoogle Scholar
  35. Servais P, Passerat J (2009) Antimicrobial resistance of fecal bacteria in waters of the Seine river watershed (France). Sci Total Environ 408:365–372CrossRefGoogle Scholar
  36. Sköld O (2000) Sulfonamide resistance: mechanisms and trends. Drug Resist Update 3(3):155–160CrossRefGoogle Scholar
  37. Smith MS, Yang RK, Knapp CW, Niu Y, Peak NM, Hanfelt MM et al (2004) Quantification of tetracycline resistance genes in feedlot lagoons using real-time PCR. Appl Environ Microb 70:7372–7377CrossRefGoogle Scholar
  38. Stepanauskas R, Glenn TC, Jagoe CH, Tuckfield RC, Lindell AH, King CJ et al (2006) Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. Environ Microbiol 8:1510–1514CrossRefGoogle Scholar
  39. Zhang XX, Zhang T (2011) Occurrence, abundance, and diversity of tetracycline resistance genes in 15 sewage treatment plants across China and other global locations. Environ Sci Technol 45:2598–2604CrossRefGoogle Scholar
  40. Zhang T, Zhang M, Zhang X, Fang HH (2009a) Tetracycline resistance genes and tetracycline resistant lactose-fermenting Enterobacteriaceae in activated sludge of sewage treatment plants. Environ Sci Technol 43(10):3455–3460CrossRefGoogle Scholar
  41. Zhang YL, Marrs CF, Simon C, Xi CW (2009b) Wastewater treatment contributes to selective increase of antibiotic resistance among Acinetobacter spp. Sci Total Environ 407:3702–3706CrossRefGoogle Scholar
  42. Zhang XX, Zhang T, Zhang M, Fang H, Cheng SP (2009c) Characterization and quantification of class 1 integrons and associated gene cassettes in sewage treatment plants. Appl Microbiol Biot 82(6):1169–1177CrossRefGoogle Scholar
  43. Zhu YG, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci U S A 110(9):3435–3440CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Jianan Li
    • 1
  • Weixiao Cheng
    • 1
  • Like Xu
    • 1
  • P. J. Strong
    • 2
  • Hong Chen
    • 1
    Email author
  1. 1.Department of Environmental Engineering, College of Environmental and Resource SciencesZhejiang UniversityHangzhouPeople’s Republic of China
  2. 2.Centre for Solid Waste Bioprocessing, School of Civil Engineering and School of Chemical EngineeringThe University of QueenslandBrisbaneAustralia

Personalised recommendations