Influence of reclaimed water discharge on the dissemination and relationships of sulfonamide, sulfonamide resistance genes along the Chaobai River, Beijing

  • Ning Zhang
  • Xiang Liu
  • Rui Liu
  • Tao Zhang
  • Miao Li
  • Zhuoran Zhang
  • Zitao Qu
  • Ziting Yuan
  • Hechun Yu
Research Article


Reclaimed water represents an important source of antibiotics and antibiotic resistance genes, threatening the ecological safety of receiving environments, while alleviating water resource shortages. This study investigated the dissemination of sulfonamide (SAs), sulfonamide resistance genes (SRGs), and class one integrons (intI1) in the surface water of the recharging area of the Chaobai River. The three antibiotics sulfamethoxazole, trimethoprim, and sulfadiazine had the highest abundance. The highest absolute abundances were 2.91×106, 6.94×106, and 2.18×104 copies/mL for sul1, sul2, and intI1 at the recharge point, respectively. SRGs and intI1 were widespread and had high abundance not only at the recharging point, but also in remote areas up to 8 km away. Seasonal variations of SRGs abundance followed the order of summer>autumn>spring>winter. Significant correlations were found between SRGs and intI1 (R2 = 0.887 and 0.786, p<0.01), indicating the potential risk of SRGs dissemination. Strong correlations between the abundance of SRGs and environmental factors were also found, suggesting that appropriate environmental conditions favor the spread of SRGs. The obtained results indicate that recharging with reclaimed water causes dissemination and enrichment of SAs and SRGs in the receiving river. Further research is required for the risk assessment and scientific management of reclaimed water.


Sulfonamide residues Sulfonamide resistance genes Reclaimed water recharge Surface water Class one integrons 



The authors would like to thank the National Natural Science Foundation of China (Grant No. 51378287) for the financial support of this work.

Supplementary material

11783_2019_1099_MOESM1_ESM.pdf (199 kb)
Supplementary material, approximately 200 KB.


  1. Amos G C A, Gozzard E, Carter C E, Mead A, Bowes MJ, Hawkey PM, Zhang L, Singer A C, Gaze W H, Wellington E M H (2015). Validated predictive modelling of the environmental resistome. The ISME Journal, 9(6): 1467–1476CrossRefGoogle Scholar
  2. Awad Y M, Kim K R, Kim S C, Kim K, Lee S R, Lee S S, Ok Y S (2015). Monitoring antibiotic residues and corresponding antibiotic resistance genes in an agroecosystem. Journal of Chemistry, 2015: 974843CrossRefGoogle Scholar
  3. Balzer F, Zühlke S, Hannappel S (2016). Antibiotics in groundwater under locations with high livestock density in Germany. Water Science and Technology: Water Supply, 16(5): 1361–1369Google Scholar
  4. Baquero F, Martinez J L, Cantón R (2008). Antibiotics and antibiotic resistance in water environments. Current Opinion in Biotechnology, 19(3): 260–265CrossRefGoogle Scholar
  5. Ben W, Wang J, Cao R, Yang M, Zhang Y, Qiang Z (2017). Distribution of antibiotic resistance in the effluents of ten municipal wastewater treatment plants in China and the effect of treatment processes. Chemosphere, 172: 392–398CrossRefGoogle Scholar
  6. Cambray G, Guerout A M, Mazel D (2010). Integrons. Annual Review of Genetics, 44(1): 141–166CrossRefGoogle Scholar
  7. Chen B, Liang X, Huang X, Zhang T, Li X (2013). Differentiating anthropogenic impacts on ARGs in the Pearl River Estuary by using suitable gene indicators. Water Research, 47(8): 2811–2820CrossRefGoogle Scholar
  8. Chen C, Li J, Chen P, Ding R, Zhang P, Li X (2014). Occurrence of antibiotics and antibiotic resistances in soils from wastewater irrigation areas in Beijing and Tianjin, China. Environmental Pollution, 193: 94–101CrossRefGoogle Scholar
  9. Chen D J, Hu M P, Wang J H, Guo Y, Dahlgren R A (2016). Factors controlling phosphorus export from agricultural/forest and residential systems to rivers in eastern China, 1980–2011. Journal of Hydrology (Amsterdam), 533: 53–61CrossRefGoogle Scholar
  10. Coutu S, Wyrsch V, Wynn H K, Rossi L, Barry D A (2013). Temporal dynamics of antibiotics in wastewater treatment plant influent. Science of the Total Environment, 458–460: 20–26CrossRefGoogle Scholar
  11. Czekalski N, Gascón Díez E, Bürgmann H (2014). Wastewater as a point source of antibiotic-resistance genes in the sediment of a freshwater lake. The ISME Journal, 8(7): 1381–1390CrossRefGoogle Scholar
  12. Devarajan N, Laffite A, Mulaji C K, Otamonga J P, Mpiana P T, Mubedi J I, Prabakar K, Ibelings BW, Poté J (2016). Occurrence of antibiotic resistance genes and bacterial markers in a tropical river receiving hospital and urban wastewaters. PLoS One, 11(2): e0149211CrossRefGoogle Scholar
  13. Di Cesare A, Eckert E M, Rogora M, Corno G (2017). Rainfall increases the abundance of antibiotic resistance genes within a riverine microbial community. Environmental Pollution, 226: 473–478CrossRefGoogle Scholar
  14. Du J, Ren H, Geng J, Zhang Y, Xu K, Ding L (2014). Occurrence and abundance of tetracycline, sulfonamide resistance genes, and class 1 integron in five wastewater treatment plants. Environmental Science and Pollution Research International, 21(12): 7276–7284CrossRefGoogle Scholar
  15. Gao P, Mao D, Luo Y, Wang L, Xu B, Xu L (2012). Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Research, 46(7): 2355–2364CrossRefGoogle Scholar
  16. Gillings M R, Gaze W H, Pruden A, Smalla K, Tiedje J M, Zhu Y G (2015). Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. The ISME Journal, 9(6): 1269–1279CrossRefGoogle Scholar
  17. Gullberg E, Cao S, Berg O G, Ilbäck C, Sandegren L, Hughes D, Andersson D I (2011). Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathogens, 7(7): e1002158CrossRefGoogle Scholar
  18. Guo M T, Yuan Q B, Yang J (2015). Distinguishing effects of ultraviolet exposure and chlorination on the horizontal transfer of antibiotic resistance genes in municipal wastewater. Environmental Science & Technology, 49(9): 5771–5778CrossRefGoogle Scholar
  19. He L Y, Liu Y S, Su H C, Zhao J L, Liu S S, Chen J, LiuWR, Ying G G (2014). Dissemination of antibiotic resistance genes in representative broiler feedlots environments: Identification of indicator ARGs and correlations with environmental variables. Environmental Science & Technology, 48(22): 13120–13129CrossRefGoogle Scholar
  20. Janke B D, Finlay J C, Hobbie S E, Baker L A, Sterner RW, Nidzgorski D, Wilson B N (2014). Contrasting influences of stormflow and baseflow pathways on nitrogen and phosphorus export from an urban watershed. Biogeochemistry, 121(1): 209–228CrossRefGoogle Scholar
  21. Jiang L, Hu X, Xu T, Zhang H, Sheng D, Yin D (2013). Prevalence of antibiotic resistance genes and their relationship with antibiotics in the Huangpu River and the drinking water sources, Shanghai, China. Science of the Total Environment, 458–460: 267–272CrossRefGoogle Scholar
  22. Jiang L, Hu X, Yin D, Zhang H, Yu Z (2011). Occurrence, distribution and seasonal variation of antibiotics in the Huangpu River, Shanghai, China. Chemosphere, 82(6): 822–828CrossRefGoogle Scholar
  23. Jiao Y N, Chen H, Gao R X, Zhu Y G, Rensing C (2017). Organic compounds stimulate horizontal transfer of antibiotic resistance genes in mixed wastewater treatment systems. Chemosphere, 184: 53–61CrossRefGoogle Scholar
  24. Karthikeyan K G, Meyer M T (2006). Occurrence of antibiotics in wastewater treatment facilities in Wisconsin, USA. Science of the Total Environment, 361(1–3): 196–207CrossRefGoogle Scholar
  25. Kim S C, Carlson K (2007). Temporal and spatial trends in the occurrence of human and veterinary antibiotics in aqueous and river sediment matrices. Environmental Science & Technology, 41(1): 50–57CrossRefGoogle Scholar
  26. Klümper U, Dechesne A, Riber L, Brandt K K, Gülay A, Sørensen S J, Smets B F (2017). Metal stressors consistently modulate bacterial conjugal plasmid uptake potential in a phylogenetically conserved manner. The ISME Journal, 11(1): 152–165CrossRefGoogle Scholar
  27. Koczura R, Mokracka J, Taraszewska A, Lopacinska N (2016). Abundance of class 1 integron-integrase and sulfonamide resistance genes in river water and sediment is affected by anthropogenic pressure and environmental factors. Microbial Ecology, 72(4): 909–916CrossRefGoogle Scholar
  28. Kümmerer K (2009). Antibiotics in the aquatic environment: A review—Part I. Chemosphere, 75(4): 417–434CrossRefGoogle Scholar
  29. Laht M, Karkman A, Voolaid V, Ritz C, Tenson T, Virta M, Kisand V (2014). Abundances of tetracycline, sulphonamide and beta-lactam antibiotic resistance genes in conventional wastewater treatment plants (WWTPs) with different waste load. PLoS One, 9(8): e103705CrossRefGoogle Scholar
  30. Lamshöft M, Sukul P, Zühlke S, Spiteller M (2007). Metabolism of 14Clabelled and non-labelled sulfadiazine after administration to pigs. Analytical and Bioanalytical Chemistry, 388(8): 1733–1745CrossRefGoogle Scholar
  31. Li J, Cheng W, Xu L, Strong P J, Chen H (2015). Antibiotic-resistant genes and antibiotic-resistant bacteria in the effluent of urban residential areas, hospitals, and a municipal wastewater treatment plant system. Environmental Science and Pollution Research International, 22(6): 4587–4596CrossRefGoogle Scholar
  32. Ling A L, Pace N R, Hernandez M T, LaPara T M (2013). Tetracycline resistance and Class 1 integron genes associated with indoor and outdoor aerosols. Environmental Science & Technology, 47(9): 4046–4052CrossRefGoogle Scholar
  33. Luo Y, Mao D, Rysz M, Zhou Q, Zhang H, Xu L, AlvarezP J J (2010). Trends in antibiotic resistance genes occurrence in the Haihe River, China. Environmental Science & Technology, 44(19): 7220–7225CrossRefGoogle Scholar
  34. Ma L, Li A D, Yin X L, Zhang T (2017). The prevalence of integrons as the carrier of antibiotic resistance genes in natural and man-made environments. Environmental Science & Technology, 51(10): 5721–5728CrossRefGoogle Scholar
  35. Ma L, Zhang X X, Zhao F, Wu B, Cheng S, Yang L (2013). Sewage treatment plant serves as a hot-spot reservoir of integrons and gene cassettes. Journal of Environmental Biology, 34(2 Spec No suppl): 391–399Google Scholar
  36. Ma Y, Li M, Wu M, Li Z, Liu X (2015). Occurrences and regional distributions of 20 antibiotics in water bodies during groundwater recharge. Science of the Total Environment, 518–519: 498–506CrossRefGoogle Scholar
  37. Makowska N, Koczura R, Mokracka J (2016). Class 1 integrase, sulfonamide and tetracycline resistance genes in wastewater treatment plant and surface water. Chemosphere, 144: 1665–1673CrossRefGoogle Scholar
  38. Mao D, Luo Y, Mathieu J, Wang Q, Feng L, Mu Q, Feng C, Alvarez P J (2014). Persistence of extracellular DNA in river sediment facilitates antibiotic resistance gene propagation. Environmental Science & Technology, 48(1): 71–78CrossRefGoogle Scholar
  39. Marti E, Jofre J, Balcazar J L (2013). Prevalence of antibiotic resistance genes and bacterial community composition in a river influenced by a wastewater treatment plant. PLoS One, 8(10): e78906CrossRefGoogle Scholar
  40. Martinez J L (2009). The role of natural environments in the evolution of resistance traits in pathogenic bacteria. Proceedings of the Royal Society of London, B: Biological Sciences, 276(1667): 2521–2530CrossRefGoogle Scholar
  41. Martinez J L, Coque T M, Baquero F (2015). What is a resistance gene? Ranking risk in resistomes. Nature Reviews. Microbiology, 13(2): 116–123CrossRefGoogle Scholar
  42. Mazel D (2006). Integrons: Agents of bacterial evolution. Nature Reviews. Microbiology, 4(8): 608–620CrossRefGoogle Scholar
  43. Mokracka J, Koczura R, Kaznowski A (2012). Multiresistant Enterobacteriaceae with class 1 and class 2 integrons in a municipal wastewater treatment plant. Water Research, 46(10): 3353–3363CrossRefGoogle Scholar
  44. Na G, Zhang W, Zhou S, Gao H, Lu Z, Wu X, Li R, Qiu L, Cai Y, Yao Z (2014). Sulfonamide antibiotics in the Northern Yellow Sea are related to resistant bacteria: implications for antibiotic resistance genes. Marine Pollution Bulletin, 84(1–2): 70–75CrossRefGoogle Scholar
  45. Partridge S R, Tsafnat G, Coiera E, Iredell J R (2009). Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiology Reviews, 33(4): 757–784CrossRefGoogle Scholar
  46. Proia L, von Schiller D, Sànchez-Melsió A, Sabater S, Borrego C M, Rodríguez-Mozaz S, Balcázar J L (2016). Occurrence and persistence of antibiotic resistance genes in river biofilms after wastewater inputs in small rivers. Environmental Pollution, 210: 121–128CrossRefGoogle Scholar
  47. Pruden A, Arabi M, Storteboom H N (2012). Correlation between upstream human activities and riverine antibiotic resistance genes. Environmental Science & Technology, 46(21): 11541–11549CrossRefGoogle Scholar
  48. Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy M C, Michael I, Fatta-Kassinos D (2013). Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: A review. Science of the Total Environment, 447: 345–360CrossRefGoogle Scholar
  49. Rodriguez-Mozaz S, Chamorro S, Marti E, Huerta B, Gros M, Sànchez-Melsió A, Borrego C M, Barceló D, Balcázar J L (2015). Occurrence of antibiotics and antibiotic resistance genes in hospital and urban wastewaters and their impact on the receiving river. Water Research, 69: 234–242CrossRefGoogle Scholar
  50. Sabri N A, Schmitt H, Van der Zaan B, Gerritsen H W, Zuidema T, Rijnaarts H H M (2018). Prevalence of antibiotics and antibiotic resistance genes in a wastewater effluent-receiving river in the Netherlands. Journal of Environmental Chemical Engineering (Online), available online at (accessed March 2, 2018)Google Scholar
  51. Tolls J (2001). Sorption of veterinary pharmaceuticals in soils: A review. Environmental Science & Technology, 35(17): 3397–3406CrossRefGoogle Scholar
  52. Wang J, Ben W, Zhang Y, Yang M, Qiang Z (2015). Effects of thermophilic composting on oxytetracycline, sulfamethazine, and their corresponding resistance genes in swine manure. Environmental Science. Processes & Impacts, 17(9): 1654–1660CrossRefGoogle Scholar
  53. Wu N, Qiao M, Zhang B, Cheng W D, Zhu Y G (2010). Abundance and diversity of tetracycline resistance genes in soils adjacent to representative swine feedlots in China. Environmental Science & Technology, 44(18): 6933–6939CrossRefGoogle Scholar
  54. Xu J, Xu Y, Wang H, Guo C, Qiu H, He Y, Zhang Y, Li X, Meng W (2015). Occurrence of antibiotics and antibiotic resistance genes in a sewage treatment plant and its effluent-receiving river. Chemosphere, 119: 1379–1385CrossRefGoogle Scholar
  55. Xu W H, Zhang G, Zou S C, Li X D, Liu Y C (2007). Determination of selected antibiotics in the Victoria Harbour and the Pearl River, South China using high-performance liquid chromatography-electrospray ionization tandem mass spectrometry. Environmental Pollution, 145 (3): 672–679CrossRefGoogle Scholar
  56. Xu Y, Guo C, Luo Y, Lv J, Zhang Y, Lin H, Wang L, Xu J (2016). Occurrence and distribution of antibiotics, antibiotic resistance genes in the urban rivers in Beijing, China. Environmental Pollution, 213: 833–840CrossRefGoogle Scholar
  57. Yang J F, Ying G G, Zhao J L, Tao R, Su H C, Liu Y S (2011). Spatial and seasonal distribution of selected antibiotics in surface waters of the Pearl Rivers, China. Journal of Environmental Science and Health. Part. B, Pesticides, Food Contaminants, and Agricultural Wastes, 46(3): 272–280CrossRefGoogle Scholar
  58. Yuan X, Qiang Z, Ben W, Zhu B, Qu J (2015). Distribution, mass load and environmental impact of multiple-class pharmaceuticals in conventional and upgraded municipal wastewater treatment plants in East China. Environmental Science. Processes & Impacts, 17(3): 596–605CrossRefGoogle Scholar
  59. Zhang X, Wu B, Zhang Y, Zhang T, Yang L, Fang H H, Ford T, Cheng S (2009). Class 1 integronase gene and tetracycline resistance genes tetA and tetC in different water environments of Jiangsu Province, China. Ecotoxicology (London, England), 18(6): 652–660CrossRefGoogle Scholar
  60. Zhang X X, Zhang T (2011). Occurrence, abundance, and diversity of tetracycline resistance genes in 15 sewage treatment plants across China and other global locations. Environmental Science & Technology, 45(7): 2598–2604CrossRefGoogle Scholar
  61. Zhan X M, Xiao L W (2017). Livestock Waste 2016-International Conference on Recent Advances in Pollution Control and Resource Recovery for the Livestock Sector. Frontiers of Environmental Science & Engineering, 11(3): 16CrossRefGoogle Scholar
  62. Zhang J, Wei Z, Jia H F, Huang X (2017). Factors influencing water quality indices in a typical urban river originated with reclaimed water. Frontiers of Environmental Science & Engineering, 11(4):8CrossRefGoogle Scholar
  63. Zhang Y, Li A, Dai T, Li F, Xie H, Chen L, Wen D (2018). Cell-free DNA: A neglected source for antibiotic resistance genes spreading from WWTPs. Environmental Science & Technology, 52(1): 248–257CrossRefGoogle Scholar
  64. Zou S, Xu W, Zhang R, Tang J, Chen Y, Zhang G (2011). Occurrence and distribution of antibiotics in coastal water of the Bohai Bay, China: Impacts of river discharge and aquaculture activities. Environmental Pollution, 159(10): 2913–2920CrossRefGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Ning Zhang
    • 1
    • 2
  • Xiang Liu
    • 1
  • Rui Liu
    • 1
  • Tao Zhang
    • 3
  • Miao Li
    • 1
  • Zhuoran Zhang
    • 1
  • Zitao Qu
    • 4
  • Ziting Yuan
    • 5
  • Hechun Yu
    • 5
  1. 1.School of EnvironmentTsinghua UniversityBeijingChina
  2. 2.Division of Environment and Resources Research, Transport Planning and Research InstituteMinistry of TransportBeijingChina
  3. 3.Chinese Academy for Environmental PlanningBeijingChina
  4. 4.Institute of Chemistry, Industrial ChemistryTechnical University of Munich (Asian Campus)SingaporeSingapore
  5. 5.School of Water Resources and EnvironmentChina University of Geosciences (Beijing)BeijingChina

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