Skip to main content
SpringerLink
Log in

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

  • Research Article
  • Published:
Frontiers of Environmental Science & Engineering Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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): 1467–1476

    CAS  Google Scholar 

  • 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: 974843

    Google Scholar 

  • 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): 1361–1369

    CAS  Google Scholar 

  • Baquero F, Martinez J L, Cantón R (2008). Antibiotics and antibiotic resistance in water environments. Current Opinion in Biotechnology, 19(3): 260–265

    CAS  Google Scholar 

  • 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: 392–398

    CAS  Google Scholar 

  • Cambray G, Guerout A M, Mazel D (2010). Integrons. Annual Review of Genetics, 44(1): 141–166

    CAS  Google Scholar 

  • 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): 2811–2820

    CAS  Google Scholar 

  • 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: 94–101

    CAS  Google Scholar 

  • 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: 53–61

    CAS  Google Scholar 

  • 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: 20–26

    Google Scholar 

  • 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): 1381–1390

    CAS  Google Scholar 

  • 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): e0149211

    Google Scholar 

  • 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: 473–478

    Google Scholar 

  • 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): 7276–7284

    CAS  Google Scholar 

  • 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): 2355–2364

    CAS  Google Scholar 

  • 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): 1269–1279

    CAS  Google Scholar 

  • 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): e1002158

    CAS  Google Scholar 

  • 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): 5771–5778

    CAS  Google Scholar 

  • 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): 13120–13129

    CAS  Google Scholar 

  • 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): 209–228

    CAS  Google Scholar 

  • 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: 267–272

    Google Scholar 

  • 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): 822–828

    CAS  Google Scholar 

  • 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: 53–61

    CAS  Google Scholar 

  • 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): 196–207

    CAS  Google Scholar 

  • 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): 50–57

    CAS  Google Scholar 

  • 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): 152–165

    Google Scholar 

  • 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): 909–916

    CAS  Google Scholar 

  • Kümmerer K (2009). Antibiotics in the aquatic environment: A review—Part I. Chemosphere, 75(4): 417–434

    Google Scholar 

  • 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): e103705

    Google Scholar 

  • 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): 1733–1745

    Google Scholar 

  • 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): 4587–4596

    CAS  Google Scholar 

  • 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): 4046–4052

    CAS  Google Scholar 

  • 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): 7220–7225

    Google Scholar 

  • 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): 5721–5728

    CAS  Google Scholar 

  • 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): 391–399

    CAS  Google Scholar 

  • 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: 498–506

    Google Scholar 

  • Makowska N, Koczura R, Mokracka J (2016). Class 1 integrase, sulfonamide and tetracycline resistance genes in wastewater treatment plant and surface water. Chemosphere, 144: 1665–1673

    CAS  Google Scholar 

  • 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): 71–78

    CAS  Google Scholar 

  • 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): e78906

    CAS  Google Scholar 

  • 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): 2521–2530

    Google Scholar 

  • Martinez J L, Coque T M, Baquero F (2015). What is a resistance gene? Ranking risk in resistomes. Nature Reviews. Microbiology, 13(2): 116–123

    CAS  Google Scholar 

  • Mazel D (2006). Integrons: Agents of bacterial evolution. Nature Reviews. Microbiology, 4(8): 608–620

    CAS  Google Scholar 

  • 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): 3353–3363

    CAS  Google Scholar 

  • 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): 70–75

    CAS  Google Scholar 

  • 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): 757–784

    CAS  Google Scholar 

  • 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: 121–128

    CAS  Google Scholar 

  • Pruden A, Arabi M, Storteboom H N (2012). Correlation between upstream human activities and riverine antibiotic resistance genes. Environmental Science & Technology, 46(21): 11541–11549

    CAS  Google Scholar 

  • 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: 345–360

    CAS  Google Scholar 

  • 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: 234–242

    CAS  Google Scholar 

  • 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 https://doi.org/10.1016/j.jece.2018.03.004 (accessed March 2, 2018)

    Google Scholar 

  • Tolls J (2001). Sorption of veterinary pharmaceuticals in soils: A review. Environmental Science & Technology, 35(17): 3397–3406

    CAS  Google Scholar 

  • 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): 1654–1660

    Google Scholar 

  • 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): 6933–6939

    CAS  Google Scholar 

  • 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: 1379–1385

    CAS  Google Scholar 

  • 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): 672–679

    CAS  Google Scholar 

  • 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: 833–840

    CAS  Google Scholar 

  • 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): 272–280

    Google Scholar 

  • 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): 596–605

    Google Scholar 

  • 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): 652–660

    CAS  Google Scholar 

  • 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): 2598–2604

    CAS  Google Scholar 

  • 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): 16

    Google Scholar 

  • 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):8

    Google Scholar 

  • 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): 248–257

    CAS  Google Scholar 

  • 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): 2913–2920

    CAS  Google Scholar 

Download references

Acknowledgements

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

Author information

Authors and Affiliations

  1. School of Environment, Tsinghua University, Beijing, 100084, China

    Ning Zhang, Xiang Liu, Rui Liu, Miao Li & Zhuoran Zhang

  2. Division of Environment and Resources Research, Transport Planning and Research Institute, Ministry of Transport, Beijing, 100028, China

    Ning Zhang

  3. Chinese Academy for Environmental Planning, Beijing, 100012, China

    Tao Zhang

  4. Institute of Chemistry, Industrial Chemistry, Technical University of Munich (Asian Campus), Singapore, 139660, Singapore

    Zitao Qu

  5. School of Water Resources and Environment, China University of Geosciences (Beijing), Beijing, 100083, China

    Ziting Yuan & Hechun Yu

Authors
  1. Ning Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhuoran Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zitao Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ziting Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hechun Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xiang Liu or Miao Li.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, N., Liu, X., Liu, R. et al. Influence of reclaimed water discharge on the dissemination and relationships of sulfonamide, sulfonamide resistance genes along the Chaobai River, Beijing. Front. Environ. Sci. Eng. 13, 8 (2019). https://doi.org/10.1007/s11783-019-1099-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11783-019-1099-2

Keywords

Search

Navigation