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

Abstract

Reclaimed water threatens the ecological safety of the Chaobai River.

SMX, TMP, and SDZ were the first three abundant antibiotics in the research area.

SRGs and intI1 were widespread with high abundance after reclaimed water recharge.

The SRGs values followed the sequence: Summer>autumn>spring>winter.

Strong correlations were detected between SRGs and environmental factors.

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.

Graphical abstract

Keywords

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

References

[1] Amos G C A, Gozzard E, Carter C E, Mead A, Bowes M J, Hawkey P M, 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

[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: 974843

[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): 1361–1369

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

[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: 392–398

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

[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): 2811–2820

[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: 94–101

[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: 53–61

[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: 20–26

[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): 1381–1390

[12] Devarajan N, Laffite A, Mulaji C K, Otamonga J P, Mpiana P T, Mubedi J I, Prabakar K, Ibelings B W, 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

[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: 473–478

[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): 7276–7284

[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): 2355–2364

[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): 1269–1279

[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): e1002158

[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): 5771–5778

[19] He L Y, Liu Y S, Su H C, Zhao J L, Liu S S, Chen J, Liu W R, 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

[20] Janke B D, Finlay J C, Hobbie S E, Baker L A, Sterner R W, 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

[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: 267–272

[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): 822–828

[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: 53–61

[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): 196–207

[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): 50–57

[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): 152–165

[27] Koczura R, Mokracka J, Taraszewska A, Łopacinska 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

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

[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): e103705

[30] Lamshöft M, Sukul P, Zühlke S, Spiteller M (2007). Metabolism of 14C-labelled and non-labelled sulfadiazine after administration to pigs. Analytical and Bioanalytical Chemistry, 388(8): 1733–1745

[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): 4587–4596

[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): 4046–4052

[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): 7220–7225

[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): 5721–5728

[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): 391–399

[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: 498–506

[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: 1665–1673

[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): 71–78

[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): e78906

[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): 2521–2530

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

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

[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): 3353–3363

[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): 70–75

[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): 757–784

[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: 121–128

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

[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: 345–360

[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: 234–242

[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),accessed March 2, 2018)

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

[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): 1654–1660

[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): 6933–6939

[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: 1379–1385

[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): 672–679

[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: 833–840

[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): 272–280

[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): 596–605

[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): 652–660

[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): 2598–2604

[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): 16

[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):8

[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): 248–257

[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): 2913–2920

RIGHTS & PERMISSIONS

Higher Education Press and Springer–Verlag GmbH Germany, part of Springer Nature