Presence, dissemination and removal of antibiotic resistant bacteria and antibiotic resistance genes in urban drinking water system: A review

Highlights

Reviewed the change of ARGs and ARB in full-scale urban drinking water systems.

Conventional processes are more promising than BAC process in ARGs removal.

Mechanisms of ARGs enrichment and spread in BAC filter and DWDSs are discussed.

Raise the need of future research on ARGs and ARB change in building plumbing systems.

Abstract

Antibiotic resistance in aquatic environment has become an important pollution problem worldwide. In recent years, much attention was paid to antibiotic resistance in urban drinking water systems due to its close relationship with the biosafety of drinking water. This review was focused on the mechanisms of antibiotic resistance, as well as the presence, dissemination and removal of antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARGs) in the urban drinking water system. First, the presence of ARB and ARGs in the drinking water source was discussed. The variation of concentration of ARGs and ARB during coagulation, sedimentation and filtration process were provided subsequently, in which filtration was proved to be a promising technology to remove ARGs. However, biological activated carbon (BAC) process and drinking water distribution systems (DWDSs) could be incubators which promote the antibiotic resistance, due to the enrichment of ARGs and ARB in the biofilms attached to the active carbon and pipe wall. Besides, as for disinfection process, mechanisms of the inactivation of ARB and the promotion of conjugative transfer of ARGs under chlorine, ozone and UV disinfection were described in detail. Here we provide some theoretical support for future researches which aim at antibiotic resistance controlling in drinking water.

Graphical abstract

Keywords

Antibiotic resistant bacteria / Antibiotic resistance genes / Water source / Drinking water treatment plant / Drinking water distribution system / Urban drinking water system

References

[1] Aguilar M I, Sáez J, Lloréns M, Soler A, Ortuño J F (2002). Nutrient removal and sludge production in the coagulation-flocculation process. Water Research, 36(11): 2910–2919

[2] Alizadeh Fard M, Barkdoll B D (2018). Stagnation reduction in drinking water storage tanks through internal piping with implications for water quality improvement. Journal of Hydraulic Engineering, 144(5): 05018004

[3] Allen H K, Donato J, Wang H H, Cloud-Hansen K A, Davies J, Handelsman J (2010). Call of the wild: Antibiotic resistance genes in natural environments. Nature Reviews. Microbiology, 8(4): 251–259

[4] Asoh N, Masaki H, Watanabe H, Watanabe K, Mitsusima H, Matsumoto K, Oishi K, Nagatake T (2005). Molecular characterization of the transmission between the colonization of methicillin-resistant Staphylococcus aureus to human and environmental contamination in geriatric long-term care wards. Internal Medicine (Tokyo, Japan), 44(1): 41–45

[5] Baker-Austin C, Wright M S, Stepanauskas R, McArthur J V (2006). Co-selection of antibiotic and metal resistance. Trends in Microbiology, 14(4): 176–182

[6] Balcázar J L, Subirats J, Borrego C M (2015). The role of biofilms as environmental reservoirs of antibiotic resistance. Frontiers in Microbiology, 6: 1216

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

[8] Berendonk T U, Manaia C M, Merlin C, Fatta-Kassinos D, Cytryn E, Walsh F, Bürgmann H, Sørum H, Norström M, Pons M N, Kreuzinger N, Huovinen P, Stefani S, Schwartz T, Kisand V, Baquero F, Martinez J L (2015). Tackling antibiotic resistance: The environmental framework. Nature Reviews. Microbiology, 13(5): 310–317

[9] 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

[10] 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

[11] Cai P, Huang Q Y, Zhang X W (2006). Interactions of DNA with clay minerals and soil colloidal particles and protection against degradation by DNase. Environmental Science & Technology, 40(9): 2971–2976

[12] Charpentier E, Tuomanen E (2000). Mechanisms of antibiotic resistance and tolerance in Streptococcus pneumoniae. Microbes and Infection, 2(15): 1855–1864

[13] Chen B, Liang X, Nie X, Huang X, Zou S, Li X (2015). The role of class I integrons in the dissemination of sulfonamide resistance genes in the Pearl River and Pearl River Estuary, South China. Journal of Hazardous Materials, 282: 61–67

[14] Chen P, Chen C, Li X (2017). Transport of antibiotic resistance plasmids in porous media and the influence of surfactants. Frontiers of Environmental Science & Engineering, 12(2): 5

[15] Chen R Z, Craik S A, Bolton J R (2009). Comparison of the action spectra and relative DNA absorbance spectra of microorganisms: information important for the determination of germicidal fluence (UV dose) in an ultraviolet disinfection of water. Water Research, 43(20): 5087–5096

[16] Davies D G, Parsek M R, Pearson J P, Iglewski B H, Costerton J W, Greenberg E P (1998). The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science, 280(5361): 295–298

[17] Davies J, Davies D (2010). Origins and evolution of antibiotic resistance. Microbiology and molecular biology reviews: MMBR, 74(3): 417–433

[18] Dodd M C (2012). Potential impacts of disinfection processes on elimination and deactivation of antibiotic resistance genes during water and wastewater treatment. Journal of environmental monitoring: JEM, 14(7): 1754–1771

[19] Durão P, Balbontín R, Gordo I (2018). Evolutionary mechanisms shaping the maintenance of antibiotic resistance. Trends in Microbiology, 26(8): 677–691

[20] Ehlers L J, Bouwer E J (1999). RP4 plasmid transfer among species of Pseudomonas in a biofilm reactor. Water Science and Technology, 39(7): 163–171

[21] Faria C, Vaz-Moreira I, Serapicos E, Nunes O C, Manaia C M (2009). Antibiotic resistance in coagulase negative staphylococci isolated from wastewater and drinking water. The Science of the total environment, 407(12): 3876–3882

[22] Fauci A S, Marston D (2014). The perpetual challenge of antimicrobial resistance. JAMA, 311(18): 1853–1854

[23] Fleming A (1929). On the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenzae. British Journal of Experimental Pathology, 10: 226–236

[24] Flemming H C, Percival S, Walker J (2002). Contamination potential of biofilms in water distribution systems. Water Science and Technology: Water Supply, 2(1): 271–280

[25] Flemming H C, Wingender J (2010). The biofilm matrix. Nature Reviews. Microbiology, 8(9): 623–633

[26] Gothwal R, Shashidhar T (2015). Antibiotic pollution in the environment: A review. Clean-Soil Air Water, 43(4): 479–489

[27] Griffiths R P, Moyer C L, Caldwell B A, Ye C, Morita R Y (1990). Long-term starvation-induced loss of antibiotic resistance in bacteria. Microbial Ecology, 19(3): 251–257

[28] 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

[29] 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. The Science of the total environment, 493: 626–631

[30] Guo X P, Yang Y, Lu D P, Niu Z S, Feng J N, Chen Y R, Tou F Y, Garner E, Xu J, Liu M, Hochella M F Jr (2018). Biofilms as a sink for antibiotic resistance genes (ARGs) in the Yangtze Estuary. Water Research, 129: 277–286

[31] Haas C N, Jacangelo J G, Bishop M M, Cameron C D, Chowdhury Z K, Connell G F, Doty G A, Finch G R, Gates D J, Greenberg A E, Hoehn R C, Huebner W B, Jensen J N, Lange A L, Long B W, Moyer N P, Nagel W H, Noran P F, Palin A T, Regli S E, Routt J C, Symons J M, Thompson C K, Voyles C F (1992). Survey of water utility disinfection practices. Journal- American Water Works Association, 84(9): 121–128

[32] 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): 2775–2781

[33] Huang J J, Hu H Y, Wu Y H, Wei B, Lu Y (2013). Effect of chlorination and ultraviolet disinfection on tetA-mediated tetracycline resistance of Escherichia coli. Chemosphere, 90(8): 2247–2253

[34] Ji P, Parks J, Edwards M A, Pruden A (2015). Impact of water chemistry, pipe material and stagnation on the building plumbing microbiome. PLoS One, 10(10): e0141087

[35] 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

[36] 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. The Science of the total environment, 458-460: 267–272

[37] Koike S, Krapac I G, Oliver H D, Yannarell A C, Chee-Sanford J C, Aminov R I, Mackie R I (2007). Monitoring and source tracking of tetracycline resistance genes in lagoons and groundwater adjacent to swine production facilities over a 3-year period. Applied and Environmental Microbiology, 73(15): 4813–4823

[38] 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

[39] Krige M (2009). Molecular investigation of the chlorine and antibiotic resistance mechanisms of Escherichia coli isolated from natural water sources in the Western Cape. Dissertation for the Doctoral Degree. Stellenbosch: University of Stellenbosch

[40] Kumarasamy K K, Toleman M A, Walsh T R, Bagaria J, Butt F, Balakrishnan R, Chaudhary U, Doumith M, Giske C G, Irfan S, Krishnan P, Kumar A V, Maharjan S, Mushtaq S, Noorie T, Paterson D L, Pearson A, Perry C, Pike R, Rao B, Ray U, Sarma J B, Sharma M, Sheridan E, Thirunarayan M A, Turton J, Upadhyay S, Warner M, Welfare W, Livermore D M, Woodford N (2010). Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: A molecular, biological, and epidemiological study. The Lancet. Infectious diseases, 10(9): 597–602

[41] LaPara T M, Burch T R, McNamara P J, Tan D T, Yan M, Eichmiller J J (2011). Tertiary-treated municipal wastewater is a significant point source of antibiotic resistance genes into Duluth-Superior Harbor. Environmental Science & Technology, 45(22): 9543–9549

[42] Li B, Zhang T (2013). Different removal behaviours of multiple trace antibiotics in municipal wastewater chlorination. Water Research, 47(9): 2970–2982

[43] Li N, Sheng G P, Lu Y Z, Zeng R J, Yu H Q (2017). Removal of antibiotic resistance genes from wastewater treatment plant effluent by coagulation. Water Research, 111: 204–212

[44] 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

[45] Ling F, Hwang C, LeChevallier M W, Andersen G L, Liu W T (2016). Core-satellite populations and seasonality of water meter biofilms in a metropolitan drinking water distribution system. The ISME journal, 10(3): 582–595

[46] Ling F, Whitaker R, LeChevallier M W, Liu W T (2018). Drinking water microbiome assembly induced by water stagnation. The ISME journal, 12(6): 1520–1531

[47] Liu L, Hu Q, Le Y, Chen G, Tong Z, Xu Q, Wang G (2017). Chlorination-mediated EPS excretion shapes early-stage biofilm formation in drinking water systems. Process Biochemistry, 55: 41–48

[48] Luo X, Jedlicka S S, Jellison K L (2017). Role of wall shear stress in cryptosporidium parvum oocyst attachment to environmental biofilms. Applied and Environmental Microbiology, 83(24): e01533–17

[49] Lv L, Jiang T, Zhang S, Yu X (2014). Exposure to mutagenic disinfection byproducts leads to increase of antibiotic resistance in Pseudomonas aeruginosa. Environmental Science & Technology, 48(14): 8188–8195

[50] Ma L, Li B, Jiang X T, Wang Y L, Xia Y, Li A D, Zhang T (2017). Catalogue of antibiotic resistome and host-tracking in drinking water deciphered by a large scale survey. Microbiome, 5(1): 154

[51] Machado A, Bordalo A A (2014). Prevalence of antibiotic resistance in bacteria isolated from drinking well water available in Guinea-Bissau (West Africa). Ecotoxicology and Environmental Safety, 106: 188–194

[52] Manaia C M (2017). Assessing the risk of antibiotic resistance transmission from the environment to humans: Non-direct proportionality between abundance and risk. Trends in Microbiology, 25(3): 173–181

[53] Mao Y, Bakken L R, Zhao L, Frostegard A (2008). Functional robustness and gene pools of a wastewater nitrification reactor: Comparison of dispersed and intact biofilms when stressed by low oxygen and low pH. FEMS Microbiology Ecology, 66(1): 167–180

[54] Miller C P (1947). Development of bacterial resistance to antibiotics. Journal of the American Medical Association, 135(12): 749–751

[55] Miller R V (2001). Environmental bacteriophage-host interactions: Factors contribution to natural transduction. Antonie van Leeuwenhoek, 79(2): 141–147

[56] 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

[57] Neville N, Jia Z (2019). Approaches to the structure-based design of Antivirulence drugs: Therapeutics for the Post-Antibiotic Era. Molecules, 24 (3): 378

[57] Nikaido H (1994). Prevention of drug access to bacterial targets: Permeability barriers and active efflux. Science, 264(5157): 382–388

[58] 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(6): 1238–1242

[60] Papenfort K, Bassler B L (2016). Quorum sensing signal-response systems in Gram-negative bacteria. Nature Reviews. Microbiology, 14(9): 576–588

[61] Proctor C R, Dai D, Edwards M A, Pruden A (2017). Interactive effects of temperature, organic carbon, and pipe material on microbiota composition and Legionella pneumophila in hot water plumbing systems. Microbiome, 5(1): 130

[62] Pruden A, Pei R, Storteboom H, Carlson K H (2006). Antibiotic resistance genes as emerging contaminants: Studies in northern Colorado. Environmental Science & Technology, 40(23): 7445–7450

[63] Robinson T P, Bu D P, Carrique-Mas J, Fèvre E M, Gilbert M, Grance D, Hay S I, Jiwakanon J, Kakkar M, Kariuki S, Laxminarayan R, Lubroth J, Magnusson U, Thi Ngoc P, Van Boeckel TP, Woolhouse MEJ (2016). Antibiotic resistance is the quintessential One Health issue. Transactions of The Royal Society of Tropical Medicine and Hygiene, 110 (7): 377–380

[63] Rossman L A, Uber J G, Grayman W M (1995). Modeling disinfectant residuals in drinking-water storage tanks. Journal of Environmental Engineering, 121(10): 752–755

[64] Salyers A, Shoemaker N B (2006). Reservoirs of antibiotic resistance genes. Animal Biotechnology, 17(2): 137–146

[65] Savage V J, Chopra I, O’Neill A J (2013). Staphylococcus aureus biofilms promote horizontal transfer of antibiotic resistance. Antimicrobial Agents and Chemotherapy, 57(4): 1968–1970

[66] Sharma V K, Johnson N, Cizmas L, McDonald T J, Kim H (2016). A review of the influence of treatment strategies on antibiotic resistant bacteria and antibiotic resistance genes. Chemosphere, 150: 702–714

[67] Shen Y, Huang C, Lin J, Wu W, Ashbolt N J, Liu W T, Nguyen T H (2017). Effect of disinfectant exposure on legionella pneumophila associated with simulated drinking water biofilms: Release, inactivation, and infectivity. Environmental Science & Technology, 51(4): 2087–2095

[68] Shen Y, Huang C, Monroy G L, Janjaroen D, Derlon N, Lin J, Espinosa-Marzal R, Morgenroth E, Boppart S A, Ashbolt N J, Liu W T, Nguyen T H (2016). Response of simulated drinking water biofilm mechanical and structural properties to long-term disinfectant exposure. Environmental Science & Technology, 50(4): 1779–1787

[69] 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

[70] Shih K L, Lederberg J (1976). Chloramine mutagenesis in Bacillus subtilis. Science, 192(4244): 1141–1143

[71] Silbergeld E K, Graham J, Price L B (2008). Industrial food animal production, antimicrobial resistance, and human health. Annual Review of Public Health, 29(1): 151–169

[72] Smith R A, M’ikanatha N M, Read A F (2015). Antibiotic resistance: A primer and call to action. Health Communication, 30(3): 309–314

[73] Sørensen S J, Bailey M, Hansen L H, Kroer N, Wuertz S (2005). Studying plasmid horizontal transfer in situ: A critical review. Nature Reviews. Microbiology, 3(9): 700–710

[74] Stewart P S (2003). Diffusion in biofilms. Journal of Bacteriology, 185(5): 1485–1491

[75] 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. The Science of the total environment, 616-617: 453–461

[76] Szewzyk U, Szewzyk R, Manz W, Schleifer K H (2000). Microbiological safety of drinking water. Annual Review of Microbiology, 54(1): 81–127

[77] Tao R, Ying G G, Su H C, Zhou H W, Sidhu J P S (2010). Detection of antibiotic resistance and tetracycline resistance genes in Enterobacteriaceae isolated from the Pearl rivers in South China. Environmental pollution (Barking, Essex: 1987), 158(6): 2101–2109

[78] Templeton M R, Oddy F, Leung W, Rogers M (2009). Chlorine and UV disinfection of ampicillin-resistant and trimethoprim-resistant Escherichia coli. Canadian Journal of Civil Engineering, 36(5): 889–894

[79] Thames C H, Pruden A, James R E, Ray P P, Knowlton K F (2012). Excretion of antibiotic resistance genes by dairy calves fed milk replacers with varying doses of antibiotics. Frontiers in Microbiology, 3: 139

[80] Van Boeckel T P, Gandra S, Ashok A, Caudron Q, Grenfell B T, Levin S A, Laxminarayan R (2014). Global antibiotic consumption 2000 to 2010: An analysis of national pharmaceutical sales data. The Lancet. Infectious Diseases, 17(9): 742–750

[81] 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 (Barking, Essex: 1987), 212: 34–40

[83] 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

[84] 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 (Barking, Essex: 1987), 213: 119–126

[85] Xu Y, Xu J, Mao D, Luo Y (2017). Effect of the selective pressure of sub-lethal level of heavy metals on the fate and distribution of ARGs in the catchment scale. Environmental pollution (Barking, Essex: 1987), 220(Pt B): 900–908

[86] Yan J, Nadell C D, Bassler B L (2017). Environmental fluctuation governs selection for plasticity in biofilm production. The ISME journal, 11(7): 1569–1577

[87] Ye Z L, Deng Y, Lou Y, Ye X, Chen S (2018). Occurrence of veterinary antibiotics in struvite recovery from swine wastewater by using a fluidized bed. Frontiers of Environmental Science & Engineering, 12(3): 7

[88] Yuan Q B, Guo M T, Yang J (2015). Fate of antibiotic resistant bacteria and genes during wastewater chlorination: Implication for antibiotic resistance control. PLoS One, 10(3): e0119403

[89] Zainal-Abideen M, Aris A, Yusof F, Abdul-Majid Z, Selamat A, Omar S I (2012). Optimizing the coagulation process in a drinking water treatment plant—Comparison between traditional and statistical experimental design jar tests. Water Science and Technology: A Journal of the International Association on Water Pollution Research, 65(3): 496–503

[90] 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

[91] 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 (Barking, Essex: 1987), 233: 132–141

[92] 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

[93] Zhang X X, Zhang T, Fang H H (2009). Antibiotic resistance genes in water environment. Applied Microbiology and Biotechnology, 82(3): 397–414

[94] Zhang Y, Gu A Z, He M, Li D, Chen J (2017). Subinhibitory concentrations of disinfectants promote the horizontal transfer of multidrug resistance genes within and across genera. Environmental Science & Technology, 51(1): 570–580

[95] Zhang Y, Zhuang Y, Geng J, Ren H, Zhang Y, Ding L, Xu K (2015). Inactivation of antibiotic resistance genes in municipal wastewater effluent by chlorination and sequential UV/chlorination disinfection. The Science of the total environment, 512-513: 125–132

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

[97] 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

We are grateful for the cooperation and participation of the utilities that were involved, which is supported by China’s National Critical Project for Science and Technology on Water Pollution Prevention and Control (No. 2017ZX07201001), Major project of Chengdu Chuanli Intelligence Fluid Equipment Co., Ltd. (No. 20182078), and Major Project of WPG (Shanghai) Smart Water Public Co., Ltd. (No. 20183231).

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