Impacts of advanced treatment processes on elimination of antibiotic resistance genes in a municipal wastewater treatment plant

Highlights

The distributions of ARGs were monitored in a WWTP in Harbin during six months.

CASS had the best removal efficacy of ARGs compared to other processes in the WWTP.

UV disinfection could effectively control the HGT.

AGAC significantly remove ARGs and organics due to its high absorption capacity.

Combination of ozone and AGAC significantly improve removal of ARGs and organics.

Abstract

Antibiotic resistance genes (ARGs) pose a serious threat to public health. Wastewater treatment plants (WWTPs) are essential for controlling the release of ARGs into the environment. This study investigated ARG distribution at every step in the treatment process of a municipal WWTP located in Harbin for six consecutive months. Changes in ARG distribution involved in two advanced secondary effluent treatment processes, ozonation and granular activated carbon (GAC) adsorption, were analyzed. Biological treatment resulted in the highest ARG removal (0.76–1.94 log reduction), followed by ultraviolet (UV) disinfection (less than 0.5-log reduction). Primary treatment could not significantly remove ARGs. ARG removal efficiency increased with an increase in the ozone dose below 40 mg/L. However, amorphous GAC (AGAC) adsorption with a hydraulic retention time (HRT) of 1 h showed better removal of ARGs, total organic carbon (TOC), total nitrogen (TN), and total phosphorus (TP) than ozonation at a 60 mg/L dose. UV treatment could efficiently reduce the relative ARG abundance, despite presenting the lowest efficiency for the reduction of absolute ARG abundance compared with GAC and ozone treatments. The combination of ozone and AGAC can significantly improve the removal of ARGs, TOC, TN and TP. These results indicate that a treatment including biological processing, ozonation, and AGAC adsorption is a promising strategy for removing ARGs and refractory organic substances from sewage.

Graphical abstract

Keywords

Antibiotic resistance genes (ARGs) / Wastewater treatment plant (WWTP) / Ultraviolet (UV) / Ozonation / Granular activated carbon (GAC)

References

[1] Alexander J, Knopp G, Dötsch A, Wieland A, Schwartz T (2016). Ozone treatment of conditioned wastewater selects antibiotic resistance genes, opportunistic bacteria, and induce strong population shifts. Science of the Total Environment, 559: 103–112

[2] Altmann J, Ruhl A S, Zietzschmann F, Jekel M (2014). Direct comparison of ozonation and adsorption onto powdered activated carbon for micropollutant removal in advanced wastewater treatment. Water Research, 55: 185–193

[3] Auerbach E A, Seyfried E E, McMahon K D (2007). Tetracycline resistance genes in activated sludge wastewater treatment plants. Water Research, 41: 1143–1151

[4] Bonvin F, Jost L, Randin L, Bonvin E, Kohn T (2016). Super-fine powdered activated carbon (SPAC) for efficient removal of micropollutants from wastewater treatment plant effluent. Water Research, 90: 90–99

[5] Börjesson S, Melin S, Matussek A, Lindgren P (2009). A seasonal study of the mecA gene and Staphylococcus aureus including methicillin-resistant S. aureus in a municipal wastewater treatment plant. Water Research, 43: 925–932

[6] Cataldo F (2006). DNA degradation with ozone. International Journal of Biological Macromolecules, 38: 248–254

[7] Chang P H, Juhrend B, Olson T M, Marrs C F, Wigginton K R (2017). Degradation of extracellular antibiotic resistance genes with UV254 treatment. Environmental Science & Technology, 51(11): 6185–6192

[8] Chen H, Zhang M (2013). Effects of advanced treatment systems on the removal of antibiotic resistance genes in wastewater treatment plants from Hangzhou, China. Environmental Science & Technology, 47: 8157–8163

[9] Czekalski N, Imminger S, Salhi E, Veljkovic M, Kleffel K, Drissner D, Hammes F, Bürgmann H, Von Gunten U (2016). Inactivation of antibiotic resistant bacteria and resistance genes by ozone: From laboratory experiments to full-scale wastewater treatment. Environmental Science & Technology, 50: 11862–11871

[10] Dietrich J P, Loge F J, Ginn T R, Başagaoglu H (2007). Inactivation of particle-associated microorganisms in wastewater disinfection: Modeling of ozone and chlorine reactive diffusive transport in polydispersed suspensions. Water Research, 41: 2189–2201

[11] Dodd M C (2012). Potential impacts of disinfection processes on elimination and deactivation of antibiotic resistance genes during water and wastewater treatment. Journal of Envormental Monitoring, 14: 1754–1771

[12] Gao P, Mao D, Luo Y, Wang L, Xu B, Xu L (2012a). Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Research, 46: 2355–2364

[13] Gao P, Munir M, Xagoraraki I (2012b). Correlation of tetracycline and sulfonamide antibiotics with corresponding resistance genes and resistant bacteria in a conventional municipal wastewater treatment plant. Science of the Total Environment, 421: 173–183

[14] Golovko O, Kumar V, Fedorova G, Randak T, Grabic R (2014). Seasonal changes in antibiotics, antidepressants/psychiatric drugs, antihistamines and lipid regulators in a wastewater treatment plant. Chemosphere, 111: 418–426

[15] Hollender J, Zimmermann S G, Koepke S, Krauss M, Mcardell C S, Ort C, Singer H, Von Gunten U, Siegrist H (2009). Elimination of organic micropollutants in a municipal wastewater treatment plant upgraded with a full-scale post-ozonation followed by sand filtration. Environmental Science & Technology, 43: 7862–7869

[16] Huang J, Hu H, Tang F, Li Y, Lu S, Lu Y (2011). Inactivation and reactivation of antibiotic-resistant bacteria by chlorination in secondary effluents of a municipal wastewater treatment plant. Water Research, 45: 2775–2781

[17] Jones C S, Osborne D J, Stanley J (1992). Enterobacterial tetracycline resistance in relation to plasmid incompatibility. Molecular and Cellular Probes, 6: 313–317

[18] Kovalova L, Siegrist H, Von Gunten U, Eugster J, Hagenbuch M, Wittmer A, Moser R, McArdell C S (2013). Elimination of micropollutants during post-treatment of hospital wastewater with powdered activated carbon, ozone, and UV. Environmental Science & Technology, 47: 7899–7908

[19] Lee J, Jeon J H, Shin J, Jang H M, Kim S, Song M S, Kim Y M (2017). Quantitative and qualitative changes in antibiotic resistance genes after passing through treatment processes in municipal wastewater treatment plants. Science of the Total Environment, 605: 906–914

[20] Lin W, Li S, Zhang S, Yu X (2016). Reduction in horizontal transfer of conjugative plasmid by UV irradiation and low-level chlorination. Water Research, 91: 331–338

[21] Luo Y, Mao D Q, Rysz M, Zhou D X, Zhang H J, Xu L, Alvarez P (2010). Trends in antibiotic resistance genes occurrence in the Haihe River, China. Environmental Science & Technology, 44(19SI): 7220–7225

[22] Mao D, Luo Y, Mathieu J, Wang Q, Feng L, Mu Q, Feng C, Alvarez P (2013). Persistence of extracellular DNA in river sediment facilitates antibiotic resistance gene propagation. Environmental Science & Technology, 48: 71–78

[23] Margot J, Kienle C, Magnet A, Weil M, Rossi L, De Alencastro L F, Abegglen C, Thonney D, Chèvre N, Schärer M (2013). Treatment of micropollutants in municipal wastewater: Ozone or powdered activated carbon? Science of the Total Environment, 461: 480–498

[24] McKinney C W, Pruden A (2012). Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environmental Science & Technology, 46: 13393–13400

[25] Oh J, Salcedo D E, Medriano C A, Kim S (2014). Comparison of different disinfection processes in the effective removal of antibiotic-resistant bacteria and genes. Journal of Environmental Sciences (China), 26: 1238–1242

[26] Osińska A, Harnisz M, Korzeniewska E (2016). Prevalence of plasmid-mediated multidrug resistance determinants in fluoroquinolone-resistant bacteria isolated from sewage and surface water. Environmental Science and Pollution Research International, 23: 10818–10831

[27] Pei R, Cha J, Carlson K H, Pruden A (2007). Response of antibiotic resistance genes (ARG) to biological treatment in dairy lagoon water. Environmental Science & Technology, 41: 5108–5113

[28] 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

[29] Rojas-Valencia M N (2011). Research on ozone application as disinfectant and action mechanisms on wastewater microorganisms. In: Mendez-Vilas A, Ed. Science Against Microbial Pathogens: Communicating Current Research and Technological Advances. Microbiology Book Series-Number 3, vol. 1. FORMATEX, Spain, 263–271

[30] Sousa J M, Macedo G, Pedrosa M, Becerra-Castro C, Castro-Silva S, Pereira M F R, Silva A M, Nunes O C, Manaia C M (2017). Ozonation and UV254 nm radiation for the removal of microorganisms and antibiotic resistance genes from urban wastewater. Journal of Hazardous Materials, 323: 434–441

[31] Sparbier K, Schubert S, Weller U, Boogen C, Kostrzewa M (2012). Matrix-assisted laser desorption ionization-time of flight mass spectrometry-based functional assay for rapid detection of resistance against-lactam antibiotics. Journal of Clinical Microbiology, 50: 927–937

[32] Stepanauskas R, Glenn T C, Jagoe C H, Tuckfield R C, Lindell A H, King C J, McArthur J V (2006). Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. Environmental Microbiology, 8: 1510–1514

[33] Szczepanowski R, Braun S, Riedel V, Schneiker S, Krahn I, Pühler A, Schlüter A (2005). The 120 592 bp IncF plasmid pRSB107 isolated from a sewage-treatment plant encodes nine different antibiotic-resistance determinants, two iron-acquisition systems and other putative virulence-associated functions. Microbiology, 151: 1095–1111

[34] Wen Q, Yang L, Duan R, Chen Z (2016). Monitoring and evaluation of antibiotic resistance genes in four municipal wastewater treatment plants in Harbin, Northeast China. Environmental Pollution, 212: 34–40

[35] Wen Q, Yang L, Zhao Y, Huang L, Chen Z (2018). Insight into effects of antibiotics on reactor performance and evolutions of antibiotic resistance genes and microbial community in a membrane reactor. Chemosphere, 197: 420–429

[36] Zhai W, Yang F, Mao D, Luo Y (2016). Fate and removal of various antibiotic resistance genes in typical pharmaceutical wastewater treatment systems. Environmental Science and Pollution Research International, 23: 12030–12038

[37] Zhang Y, Li A, Dai T, Li F, Xie H, Chen L, Wen D (2017). Cell-free DNA: A neglected source for antibiotic resistance genes spreading from WWTPs. Environmental Science & Technology, 52: 248–257

[38] Zheng J, Su C, Zhou J, Xu L, Qian Y, Chen H (2017). Effects and mechanisms of ultraviolet, chlorination, and ozone disinfection on antibiotic resistance genes in secondary effluents of municipal wastewater treatment plants. Chemical Engineering Journal, 317: 309–316

Acknowledgments

The authors greatly appreciate the financial support from the National Key R&D Program of China (No. 2018YFC0406303), and the National & Local Joint Engineering Laboratory for Municipal Sewage Resource Utilization Technology, Suzhou University of Science and Technology (No. 2018KF06). The authors declare that there are no conflicts of interest.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-019-1116-5 and is accessible for authorized users.

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