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
Influence of reclaimed water discharge on the dissemination and relationships of sulfonamide, sulfonamide resistance genes along the Chaobai River, Beijing
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.
Sulfonamide residues / Sulfonamide resistance genes / Reclaimed water recharge / Surface water / Class one integrons
[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
CrossRef
Pubmed
Google 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: 974843
CrossRef
Google 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): 1361–1369
CrossRef
Google scholar
|
[4] |
Baquero F, Martinez J L, Cantón R (2008). Antibiotics and antibiotic resistance in water environments. Current Opinion in Biotechnology, 19(3): 260–265
CrossRef
Pubmed
Google 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: 392–398
CrossRef
Pubmed
Google scholar
|
[6] |
Cambray G, Guerout A M, Mazel D (2010). Integrons. Annual Review of Genetics, 44(1): 141–166
CrossRef
Pubmed
Google 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): 2811–2820
CrossRef
Pubmed
Google 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: 94–101
CrossRef
Pubmed
Google 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: 53–61
CrossRef
Google 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: 20–26
CrossRef
Pubmed
Google 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): 1381–1390
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google 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: 473–478
CrossRef
Pubmed
Google 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): 7276–7284
CrossRef
Pubmed
Google 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): 2355–2364
CrossRef
Pubmed
Google 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): 1269–1279
CrossRef
Pubmed
Google 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): e1002158
CrossRef
Pubmed
Google 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): 5771–5778
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Google 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: 267–272
CrossRef
Pubmed
Google 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): 822–828
CrossRef
Pubmed
Google 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: 53–61
CrossRef
Pubmed
Google 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): 196–207
CrossRef
Pubmed
Google 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): 50–57
CrossRef
Pubmed
Google 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): 152–165
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google scholar
|
[28] |
Kümmerer K (2009). Antibiotics in the aquatic environment: A review—Part I. Chemosphere, 75(4): 417–434
CrossRef
Pubmed
Google 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): e103705
CrossRef
Pubmed
Google scholar
|
[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
CrossRef
Pubmed
Google 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): 4587–4596
CrossRef
Pubmed
Google 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): 4046–4052
CrossRef
Pubmed
Google 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): 7220–7225
CrossRef
Pubmed
Google 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): 5721–5728
CrossRef
Pubmed
Google 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): 391–399
Pubmed
|
[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
CrossRef
Pubmed
Google 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: 1665–1673
CrossRef
Pubmed
Google 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): 71–78
CrossRef
Pubmed
Google 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): e78906
CrossRef
Pubmed
Google 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): 2521–2530
|
[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
CrossRef
Pubmed
Google scholar
|
[42] |
Mazel D (2006). Integrons: Agents of bacterial evolution. Nature Reviews. Microbiology, 4(8): 608–620
CrossRef
Pubmed
Google 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): 3353–3363
CrossRef
Pubmed
Google 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): 70–75
CrossRef
Pubmed
Google 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): 757–784
CrossRef
Pubmed
Google 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: 121–128
CrossRef
Pubmed
Google 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): 11541–11549
CrossRef
Pubmed
Google 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: 345–360
CrossRef
Pubmed
Google 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: 234–242
CrossRef
Pubmed
Google 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 https://doi:10.1016/j.jece.2018.03.004 (accessed March 2, 2018)
|
[51] |
Tolls J (2001). Sorption of veterinary pharmaceuticals in soils: A review. Environmental Science & Technology, 35(17): 3397–3406
CrossRef
Pubmed
Google 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): 1654–1660
CrossRef
Pubmed
Google 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): 6933–6939
CrossRef
Pubmed
Google 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: 1379–1385
CrossRef
Pubmed
Google 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): 672–679
CrossRef
Pubmed
Google 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: 833–840
CrossRef
Pubmed
Google 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): 272–280
CrossRef
Pubmed
Google 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): 596–605
CrossRef
Pubmed
Google 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): 652–660
CrossRef
Pubmed
Google 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): 2598–2604
CrossRef
Pubmed
Google 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): 16
CrossRef
Google 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):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
CrossRef
Pubmed
Google 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): 2913–2920
CrossRef
Pubmed
Google scholar
|
/
〈 | 〉 |