Biofiltration and disinfection codetermine the bacterial antibiotic resistome in drinking water: A review and meta-analysis

Highlight

• Published data was used to analyze the fate of ARGs in water treatment.

• Biomass removal leads to the reduction in absolute abundance of ARGs.

• Mechanism that filter biofilm maintain ARB/ARGs was summarized.

• Potential BAR risks caused by biofiltration and chlorination were proposed.

Abstract

The bacterial antibiotic resistome (BAR) is one of the most serious contemporary medical challenges. The BAR problem in drinking water is receiving growing attention. In this study, we focused on the distribution, changes, and health risks of the BAR throughout the drinking water treatment system. We extracted the antibiotic resistance gene (ARG) data from recent publications and analyzed ARG profiles based on diversity, absolute abundance, and relative abundance. The absolute abundance of ARG was found to decrease with water treatment processes and was positively correlated with the abundance of 16S rRNA (r² = 0.963, p<0.001), indicating that the reduction of ARG concentration was accompanied by decreasing biomass. Among treatment processes, biofiltration and chlorination were discovered to play important roles in shaping the bacterial antibiotic resistome. Chlorination exhibited positive effects in controlling the diversity of ARG, while biofiltration, especially granular activated carbon filtration, increased the diversity of ARG. Both biofiltration and chlorination altered the structure of the resistome by affecting relative ARG abundance. In addition, we analyzed the mechanism behind the impact of biofiltration and chlorination on the bacterial antibiotic resistome. By intercepting influent ARG-carrying bacteria, biofilters can enrich various ARGs and maintain ARGs in biofilm. Chlorination further selects bacteria co-resistant to chlorine and antibiotics. Finally, we proposed the BAR health risks caused by biofiltration and chlorination in water treatment. To reduce potential BAR risk in drinking water, membrane filtration technology and water boiling are recommended at the point of use.

Keywords

Drinking water treatment / Antibiotic resistance gene / Biofiltration / Chlorination

参考文献

[1] Abskharon R N N, Hassan S H A, Gad El-Rab S M, Shoreit A A M (2008). Heavy metal resistant of E. coli isolated from wastewater sites in Assiut City, Egypt. Bulletin of Environmental Contamination and Toxicology, 81(3): 309–315

[2] Akinbowale O L, Peng H, Grant P, Barton M D (2007). Antibiotic and heavy metal resistance in motile aeromonads and pseudomonads from rainbow trout (Oncorhynchus mykiss) farms in Australia. International Journal of Antimicrobial Agents, 30(2): 177–182

[3] Andersson D I, Hughes D (2010). Antibiotic resistance and its cost: Is it possible to reverse resistance? Nature Reviews. Microbiology, 8(4): 260–271

[4] Andersson D I, Hughes D (2012). Evolution of antibiotic resistance at non-lethal drug concentrations. Drug Resist. Updat., 15(3): 162–172

[5] Armstrong J L, Calomiris J J, Seidler R J (1982). Selection of antibiotic-resistant standard plate count bacteria during water treatment. Applied and Environmental Microbiology, 44(2): 308–316

[6] Bagge N, Hentzer M, Andersen J B, Ciofu O, Givskov M, Høiby N (2004). Dynamics and spatial distribution of beta-lactamase expression in Pseudomonas aeruginosa biofilms. Antimicrobial Agents and Chemotherapy, 48(4): 1168–1174PMID:15047517

[7] Bai X, Ma X, Xu F, Li J, Zhang H, Xiao X (2015). The drinking water treatment process as a potential source of affecting the bacterial antibiotic resistance. Science of the Total Environment, 533: 24–31

[8] Baquero F, Negri M C, Morosini M I, Blazquez J (2008). The antibiotic selective process: concentration-specific amplification of low-level resistant populations. Antibiotic Resistance: Origins, Evolution, Selection and Spread, 207, 93

[9] Beaudoin D L, Bryers J D, Cunningham A B, Peretti S W (1998). Mobilization of broad host range plasmid from Pseudomonas putida to established biofilm of Bacillus azotoformans. I. Experiments. Biotechnology and Bioengineering, 57(3): 272–279

[10] Benotti M J, Trenholm R A, Vanderford B J, Holady J C, Stanford B D, Snyder S A (2009). Pharmaceuticals and endocrine disrupting compounds in U.S. drinking water. Environmental Science & Technology, 43(3): 597–603

[11] Bergeron S, Boopathy R, Nathaniel R, Corbin A, LaFleur G (2015). Presence of antibiotic resistant bacteria and antibiotic resistance genes in raw source water and treated drinking water. International Biodeterioration & Biodegradation, 102: 370–374

[12] Bergeron S, Raj B, Nathaniel R, Corbin A, LaFleur G (2017). Presence of antibiotic resistance genes in raw source water of a drinking water treatment plant in a rural community of USA. International Biodeterioration & Biodegradation, 124: 3–9

[13] Bernier S P, Lebeaux D, DeFrancesco A S, Valomon A, Soubigou G, Coppée J Y, Ghigo J M, Beloin C (2013). Starvation, together with the SOS response, mediates high biofilm-specific tolerance to the fluoroquinolone ofloxacin. PLoS Genetics, 9(1): e1003144

[14] Berry D, Xi C, Raskin L (2006). Microbial ecology of drinking water distribution systems. Current Opinion in Biotechnology, 17(3): 297–302

[15] Bomo A M, Stevik T K, Hovi I, Hanssen J F (2004). Bacterial removal and protozoan grazing in biological sand filters. Journal of Environmental Quality, 33(3): 1041–1047

[16] Borriello G, Werner E, Roe F, Kim A M, Ehrlich G D, Stewart P S (2004). Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms. Antimicrobial Agents and Chemotherapy, 48(7): 2659–2664

[17] Brewer W S, Carmichael W W (1979). Microbiological characterization of granular activated carbon filter systems. Journal- American Water Works Association, 71(12): 738–740

[18] Brown M R, Allison D G, Gilbert P (1988). Resistance of bacterial biofilms to antibiotics: A growth-rate related effect? J. Antimicrob. Chemother., 22(6): 777–780

[19] Bustamante H A, Shanker S R, Pashley R M, Karaman M E (2001). Interaction between Cryptosporidium oocysts and water treatment coagulants. Water Research, 35(13): 3179–3189

[20] Chao Y, Ma L, Yang Y, Ju F, Zhang X X, Wu W M, Zhang T (2013). Metagenomic analysis reveals significant changes of microbial compositions and protective functions during drinking water treatment. Scientific Reports, 3(1): 3550

[21] Chapman J S (2003). Disinfectant resistance mechanisms, cross-resistance, and co-resistance. International Biodeterioration & Biodegradation, 51(4): 271–276

[22] Chen S, Li X, Wang Y, Zeng J, Ye C, Li X, Guo L, Zhang S, Yu X (2018). Induction of Escherichia coli into a VBNC state through chlorination/chloramination and differences in characteristics of the bacterium between states. Water Research, 142: 279–288

[23] Chiang W C, Nilsson M, Jensen P Ø, Høiby N, Nielsen T E, Givskov M, Tolker-Nielsen T (2013). Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrobial Agents and Chemotherapy, 57(5): 2352–2361

[24] Christgen B, Yang Y, Ahammad S Z, Li B, Rodriquez D C, Zhang T, Graham D W (2015). Metagenomics shows that low-energy anaerobic-aerobic treatment reactors reduce antibiotic resistance gene levels from domestic wastewater. Environmental Science & Technology, 49(4): 2577–2584

[25] Conibear T C, Collins S L, Webb J S (2009). Role of mutation in Pseudomonas aeruginosa biofilm development. PLoS One, 4(7): e6289

[26] D’Alessio M, Yoneyama B, Kirs M, Kisand V, Ray C (2015). Pharmaceutically active compounds: Their removal during slow sand filtration and their impact on slow sand filtration bacterial removal. Science of the Total Environment 524-525: 124–135

[27] Dean R J, Shimmield T M, Black K D (2007). Copper, zinc and cadmium in marine cage fish farm sediments: an extensive survey. Environmental Pollution, 145(1): 84–95

[28] Devi R, Alemayehu E, Singh V, Kumar A, Mengistie E (2008). Removal of fluoride, arsenic and coliform bacteria by modified homemade filter media from drinking water. Bioresource Technology, 99(7): 2269–2274

[29] Driffield K, Miller K, Bostock J M, O’Neill A J, Chopra I (2008). Increased mutability of Pseudomonas aeruginosa in biofilms. J. Antimicrob. Chemother., 61(5): 1053–1056

[30] Du M, Chen J, Sun F, Luan X, Wang D, Li Y, Zhang X (2008). Studies of viable but nonculturable Vibrio parahaemolyticus at low temperature under poor nutrition conditions and its resuscitation. Acta Hydrobiologica Sinica, 32(2): 178

[31] Farkas A, Butiuc-Keul A, Ciatarâş D, Neamţu C, Crăciunaş C, Podar D, Drăgan-Bularda M (2013). Microbiological contamination and resistance genes in biofilms occurring during the drinking water treatment process. Science of the Total Environment, 443: 932–938

[32] Friedberg E C, Walker G C, Siede W, Wood R D (2005). DNA repair and mutagenesis. Washington, DC: American Society for Microbiology Press

[33] Garner E, Chen C, Xia K, Bowers J, Engelthaler D M, McLain J, Edwards M A, Pruden A (2018). Metagenomic characterization of antibiotic resistance genes in full-scale reclaimed water distribution systems and corresponding potable systems. Environmental Science & Technology, 52(11): 6113–6125

[34] Geisenberger O, Ammendola A, Christensen B B, Molin S, Schleifer K H, Eberl L (1999). Monitoring the conjugal transfer of plasmid RP4 in activated sludge and in situ identification of the transconjugants. FEMS Microbiology Letters, 174(1): 9–17

[35] Ghosh A, Singh A, Ramteke P W, Singh V P (2000). Characterization of large plasmids encoding resistance to toxic heavy metals in Salmonella abortus equi. Biochemical and Biophysical Research Communications, 272(1): 6–11

[36] 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

[37] 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

[38] Guo X, Li J, Yang F, Yang J, Yin D (2014). Prevalence of sulfonamide and tetracycline resistance genes in drinking water treatment plants in the Yangtze River Delta, China. Science of the Total Environment, 493: 626–631

[39] Han L, Liu W, Chen M, Zhang M, Liu S, Sun R, Fei X (2013). Comparison of NOM removal and microbial properties in up-flow/down-flow BAC filter. Water Research, 47(14): 4861–4868

[40] Hasman H, Aarestrup F M (2002). tcrB, a gene conferring transferable copper resistance in Enterococcus faecium: Occurrence, transferability, and linkage to macrolide and glycopeptide resistance. Antimicrobial Agents and Chemotherapy, 46(5): 1410–1416

[41] Hijnen W A M, Suylen G M H, Bahlman J A, Brouwer-Hanzens A, Medema G J (2010). GAC adsorption filters as barriers for viruses, bacteria and protozoan (oo)cysts in water treatment. Water Research, 44(4): 1224–1234

[42] Hill D, Rose B, Pajkos A, Robinson M, Bye P, Bell S, Elkins M, Thompson B, Macleod C, Aaron S D, Harbour C (2005). Antibiotic susceptabilities of Pseudomonas aeruginosa isolates derived from patients with cystic fibrosis under aerobic, anaerobic, and biofilm conditions. Journal of Clinical Microbiology, 43(10): 5085–5090

[43] Hoyle B D, Costerton J W (1991). Bacterial resistance to antibiotics: The role of biofilms. In: Progress in Drug Research. Boston: Birkhäuser Basel, 91–105

[44] Hu Y, Jiang L, Zhang T, Jin L, Han Q, Zhang D, Lin K, Cui C (2018). Occurrence and removal of sulfonamide antibiotics and antibiotic resistance genes in conventional and advanced drinking water treatment processes. Journal of Hazardous Materials, 360: 364–372

[45] Huang J J, Hu H Y, Tang F, Li Y, Lu S Q, Lu Y (2011). Inactivation and reactivation of antibiotic-resistant bacteria by chlorination in secondary effluents of a municipal wastewater treatment plant. Water Research, 45(9): 2775–2781PMID:21440281

[46] Icgen B, Yilmaz F (2014). Co-occurrence of antibiotic and heavy metal resistance in Kızılırmak River isolates. Bulletin of Environmental Contamination and Toxicology, 93(6): 735–743

[47] Jia S, Shi P, Hu Q, Li B, Zhang T, Zhang X X (2015). Bacterial community shift drives antibiotic resistance promotion during drinking water chlorination. Environmental Science & Technology, 49(20): 12271–12279

[48] Khan S, Beattie T K, Knapp C W (2016). Relationship between antibiotic- and disinfectant-resistance profiles in bacteria harvested from tap water. Chemosphere, 152: 132–141

[49] Korotta-Gamage S M, Sathasivan A (2017). A review: Potential and challenges of biologically activated carbon to remove natural organic matter in drinking water purification process. Chemosphere, 167: 120–138

[50] Legube B, Langlais B, Dore M (1981). Reactions of ozone with aromatics in dilute aqueous solution: Reactivity and biodegradability of oxidation products. In: Water Pollution Research and Development. Oxford: Pergamon Press, 553–570

[51] Levin B R, Lipsitch M, Perrot V, Schrag S, Antia R, Simonsen L, Moore Walker N, Stewart F M (1997). The population genetics of antibiotic resistance. Clinical Infectious Diseases, 24(Supplement 1): S9–S16

[52] Li C, Ling F, Zhang M, Liu W T, Li Y, Liu W (2017). Characterization of bacterial community dynamics in a full-scale drinking water treatment plant. Journal of Environmental Sciences (China), 51: 21–30

[53] Li G, Ben W, Ye H, Zhang D, Qiang Z (2018). Performance of ozonation and biological activated carbon in eliminating sulfonamides and sulfonamide-resistant bacteria: A pilot-scale study. Chemical Engineering Journal, 341: 327–334

[54] Lin H, Ye C, Chen S, Zhang S, Yu X (2017). Viable but non-culturable E. coli induced by low level chlorination have higher persistence to antibiotics than their culturable counterparts. Environmental Pollution, 230: 242–249

[55] Lin W, Zeng J, Wan K, Lv L, Guo L, Li X, Yu X (2018). Reduction of the fitness cost of antibiotic resistance caused by chromosomal mutations under poor nutrient conditions. Environment International, 120: 63–71

[56] Liu A, Fong A, Becket E, Yuan J, Tamae C, Medrano L, Maiz M, Wahba C, Lee C, Lee K, Tran K P, Yang H, Hoffman R M, Salih A, Miller J H (2011). Selective advantage of resistant strains at trace levels of antibiotics: A simple and ultrasensitive color test for detection of antibiotics and genotoxic agents. Antimicrobial Agents and Chemotherapy, 55(3): 1204–1210

[57] Liu J, Sun Q, Zhang C, Li H, Song W, Zhang N, Jia X (2016a). Removal of typical antibiotics in the advanced treatment process of productive drinking water. Desalination and Water Treatment, 57(24): 11386–11391

[58] Liu S, Yang H, Liu W, Zhao Y, Wang X, Xie Y (2016b). Evaluation of backwash strategies on biologically active carbon filters by using chloroacetic acids as indicator chemicals. Process Biochemistry, 51(7): 886–894

[59] Liu S S, Qu H M, Yang D, Hu H, Liu W L, Qiu Z G, Hou A M, Guo J, Li J W, Shen Z Q, Jin M (2018). Chlorine disinfection increases both intracellular and extracellular antibiotic resistance genes in a full-scale wastewater treatment plant. Water Research, 136: 131–136

[60] Liu Y, Wang C, Tyrrell G, Hrudey S E, Li X F (2009). Induction of Escherichia coli O157:H7 into the viable but non-culturable state by chloraminated water and river water, and subsequent resuscitation. Environmental Microbiology Reports, 1(2): 155–161

[61] Lu J, Tian Z, Yu J, Yang M, Zhang Y (2018). Distribution and abundance of antibiotic resistance genes in sand settling reservoirs and drinking water treatment plants across the Yellow River, China. Water (Basel), 10(3): 246

[62] Ma X, Bibby K (2017). Free chlorine and monochloramine inactivation kinetics of Aspergillus and Penicillium in drinking water. Water Research, 120: 265–271

[63] Madec J Y, Haenni M, Ponsin C, Kieffer N, Rion E, Gassilloud B (2016). Sequence type 48 Escherichia coli carrying the blaCTX-M-1 IncI1/ST3 plasmid in drinking water in France. Antimicrobial Agents and Chemotherapy, 60(10): 6430–6432

[64] Madsen J S, Burmølle M, Hansen L H, Sørensen S J (2012). The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunology and Medical Microbiology, 65(2): 183–195

[65] Mah T F (2012). Biofilm-specific antibiotic resistance. Future Microbiology, 7(9): 1061–1072

[66] Mao D, Luo Y, Mathieu J, Wang Q, Feng L, Mu Q, Feng C, Alvarez P J J (2014). Persistence of extracellular DNA in river sediment facilitates antibiotic resistance gene propagation. Environmental Science & Technology, 48(1): 71–78

[67] 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(24): 13393–13400

[68] Molin S, Tolker-Nielsen T (2003). Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Current Opinion in Biotechnology, 14(3): 255–261

[69] Murray G E, Tobin R S, Junkins B, Kushner D J (1984). Effect of chlorination on antibiotic resistance profiles of sewage-related bacteria. Applied and Environmental Microbiology, 48(1): 73–77

[70] Narciso-da-Rocha C, Vaz-Moreira I, Svensson-Stadler L, Moore E R, Manaia C M (2013). Diversity and antibiotic resistance of Acinetobacter spp. in water from the source to the tap. Applied Microbiology and Biotechnology, 97(1): 329–340

[71] Narkis N, Schneider-Rotel M (1980). Evaluation of ozone induced biodegradability of wastewater treatment plant effluent. Water Research, 14(8): 929–939

[72] Negri M C, Lipsitch M, Blázquez J, Levin B R, Baquero F (2000). Concentration-dependent selection of small phenotypic differences in TEM-lactamase-mediated antibiotic resistance. Antimicrobial Agents and Chemotherapy, 44(9): 2485–2491

[73] Nies D H (2000). Microbial heavy-metal resistance. Applied Microbiology and Biotechnology, 51: 451–460

[74] Normander B, Christensen B B, Molin S, Kroer N (1998). Effect of bacterial distribution and activity on conjugal gene transfer on the phylloplane of the bush bean (Phaseolus vulgaris). Applied and Environmental Microbiology, 64(5): 1902–1909

[75] Paulander W, Maisnier-Patin S, Andersson D I (2009). The fitness cost of streptomycin resistance depends on rpsL mutation, carbon source and RpoS (sigmaS). Genetics, 183(2): 539–546

[76] Pinto A J, Xi C, Raskin L (2012). Bacterial community structure in the drinking water microbiome is governed by filtration processes. Environmental Science & Technology, 46(16): 8851–8859

[77] Roberts A P, Pratten J, Wilson M, Mullany P (1999). Transfer of a conjugative transposon, Tn5397 in a model oral biofilm. FEMS Microbiology Letters, 177(1): 63–66

[78] Rusin P, Gerba C (2001). Association of chlorination and UV irradiation to increasing antibiotic resistance in bacteria. Reviews of Environmental Contamination and Toxicology, 171: 1–52

[79] Sakai A, Nakanishi M, Yoshiyama K, Maki H (2006). Impact of reactive oxygen species on spontaneous mutagenesis in Escherichia coli. Genes Cells, 11(7): 767–778

[80] Seiler C, Berendonk T U (2012). Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Frontiers in Microbiology, 3: 399

[81] Shi P, Jia S, Zhang X X, Zhang T, Cheng S, Li A (2013). Metagenomic insights into chlorination effects on microbial antibiotic resistance in drinking water. Water Research, 47(1): 111–120

[82] Simazaki D, Kubota R, Suzuki T, Akiba M, Nishimura T, Kunikane S (2015). Occurrence of selected pharmaceuticals at drinking water purification plants in Japan and implications for human health. Water Research, 76: 187–200

[83] Steinert M, Emödy L, Amann R, Hacker J (1997). Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii. Applied and Environmental Microbiology, 63(5): 2047–2053

[84] Su H C, Liu Y S, Pan C G, Chen J, He L Y, Ying G G (2018). Persistence of antibiotic resistance genes and bacterial community changes in drinking water treatment system: From drinking water source to tap water. Science of the Total Environment, 616-617: 453–461

[85] Summers A O, Wireman J, Vimy M J, Lorscheider F L, Marshall B, Levy S B, Bennett S, Billard L (1993). Mercury released from dental “silver” fillings provokes an increase in mercury- and antibiotic-resistant bacteria in oral and intestinal floras of primates. Antimicrobial Agents and Chemotherapy, 37(4): 825–834

[86] Tabak M, Scher K, Hartog E, Romling U, Matthews K R, Chikindas M L, Yaron S (2007). Effect of triclosan on Salmonella typhimurium at different growth stages and in biofilms. FEMS Microbiology Letters, 267(2): 200–206

[87] Tawfik El-Zanfaly H, Reasoner D J, Geldreich E E (1998). Bacteriological changes associated with granular activated carbon in a pilot water treatment plant. Water, Air, and Soil Pollution, 107(1/4): 73–80

[88] Turetgen I (2008). Induction of Viable but Nonculturable (VBNC) state and the effect of multiple subculturing on the survival of Legionella pneumophila strains in the presence of monochloramine. Annals of Microbiology, 58(1): 153–156

[89] Van Acker H, Van Dijck P, Coenye T (2014). Molecular mechanisms of antimicrobial tolerance and resistance in bacterial and fungal biofilms. Trends in Microbiology, 22(6): 326–333

[90] Walsh T R, Weeks J, Livermore D M, Toleman M A (2011). Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: An environmental point prevalence study. Lancet Infect Di, 11(5): 355–362

[91] Walters M C 3rd, Roe F, Bugnicourt A, Franklin M J, Stewart P S (2003). Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrobial Agents and Chemotherapy, 47(1): 317–323

[92] Wan K, Zhang M, Ye C, Lin W, Guo L, Chen S, Yu X (2019). Organic carbon: An overlooked factor that determines the antibiotic resistome in drinking water sand filter biofilm. Environment International, 125: 117–124

[93] Wang F, Li W, Li Y, Zhang J, Chen J, Zhang W, Wu X (2018). Molecular analysis of bacterial community in the tap water with different water ages of a drinking water distribution system. Frontiers of Environmental Science & Engineering, 12(3): 6

[94] Weber W Jr, Pirbazari M, Melson G (1978). Biological growth on activated carbon: an investigation by scanning electron microscopy. Environmental Science & Technology, 12(7): 817–819

[95] Wegrzyn G, Wegrzyn A (2002). Stress responses and replication of plasmids in bacterial cells. Microbial Cell Factories, 1(1): 2

[96] Xi C, Zhang Y, Marrs C F, Ye W, Simon C, Foxman B, Nriagu J (2009). Prevalence of antibiotic resistance in drinking water treatment and distribution systems. Applied and Environmental Microbiology, 75(17): 5714–5718

[97] Xu L, Ouyang W, Qian Y, Su C, Su J, Chen H (2016). High-throughput profiling of antibiotic resistance genes in drinking water treatment plants and distribution systems. Environmental Pollution, 213: 119–126

[98] Yang Y, Song W, Lin H, Wang W, Du L, Xing W (2018). Antibiotics and antibiotic resistance genes in global lakes: A review and meta-analysis. Environment International, 116: 60–73

[99] Ye Z, Weinberg H S, Meyer M T (2007). Trace analysis of trimethoprim and sulfonamide, macrolide, quinolone, and tetracycline antibiotics in chlorinated drinking water using liquid chromatography electrospray tandem mass spectrometry. Analytical Chemistry, 79(3): 1135–1144

[100] Yoon Y, Chung H J, Wen Di D Y, Dodd M C, Hur H G, Lee Y (2017). Inactivation efficiency of plasmid-encoded antibiotic resistance genes during water treatment with chlorine, UV, and UV/H₂O₂. Water Research, 123: 783–793

[101] Zhang D, Li W, Zhang S, Liu M, Zhao X, Zhang X (2011). Bacterial community and function of biological activated carbon filter in drinking water treatment. Biomed. Environ. Sci., 24(2): 122–131

[102] Zhang J, Li W, Chen J, Qi W, Wang F, Zhou Y (2018a). Impact of biofilm formation and detachment on the transmission of bacterial antibiotic resistance in drinking water distribution systems. Chemosphere, 203: 368–380

[103] Zhang M, Chen L, Ye C, Yu X (2018b). Co-selection of antibiotic resistance via copper shock loading on bacteria from a drinking water bio-filter. Environmental Pollution, 233: 132–141

[104] Zhang S, Ye C, Lin H, Lv L, Yu X (2015). UV disinfection induces a VBNC state in Escherichia coli and Pseudomonas aeruginosa. Environmental Science & Technology, 49(3): 1721–1728

[105] Zhang S, Lin W, Yu X (2016). Effects of full-scale advanced water treatment on antibiotic resistance genes in the Yangtze Delta area in China. FEMS Microbiology Ecology, 92(5), fiw065

[106] Zhang Y, Li A, Dai T, Li F, Xie H, Chen L, Wen D (2018c). Cell-free DNA: A neglected source for antibiotic resistance genes spreading from WWTPs. Environmental Science & Technology, 52(1): 248–257

[107] Zheng J, Chen T, Chen H (2018). Antibiotic resistome promotion in drinking water during biological activated carbon treatment: Is it influenced by quorum sensing? Science of the Total Environment, 612: 1–8

[108] Zhu X, Ye C, Wang Y, Chen L, Feng L (2019). Assessment of antibiotic resistance genes in dialysis water treatment processes. Frontiers of Environmental Science & Engineering, 13(3): 45

Acknowledgments

This research was supported by the National Key Research and Development Program of China-International collaborative project from Ministry of Science and Technology (Grant No. 2017YFE0107300), the National Science Foundation for Young Scientists of China (Grant No. 51708534), the Natural Science Foundation of China (Grant Nos. 51678551, 51678552 and 41861144023), Xiamen Municipal Bureau of Science and Technology (No. 3502Z20171003) and K.C.Wong Education Foundation.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-019-1189-1 and is accessible for authorized users.

版权

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