Abstract
Drinking water treatment techniques are used globally in the context of water security and public health, yet they are not applicable to antibiotic resistance gene (ARG) contamination. Using high-throughput quantitative PCR, we analyzed the prevalence and diversity of ARGs and mobile genetic elements (MGEs) in water supplies. A total of 224 ARGs and MGEs were detected in all sampling sites. Absolute abundance and detected number of ARGs decreased significantly (P < 0.05) in sand filter water after drinking water treatment and increased thereafter at point-of-use (household tap water). Changes in the composition and diversity of the bacterial community were observed in water samples at different steps. A significant correlation (P < 0.001) between microbial communities and ARG profiles was observed, and variance in ARG profiles could be primarily attributed to community composition (11.9%), and interaction between community composition, environmental factors and MGEs (30.7%). A network analysis was performed, and the results showed eight bacterial phyla were significantly correlated with nine different classes of ARGs, suggesting the potential bacterial host for ARGs. This study suggested that although the absolute abundance of ARGs decreased after treatment of drinking water treatment plants (DWTPs), the rebounded of ARGs in the water distribution system should not be neglected.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All relevant data are within the manuscript and available from the corresponding author upon request
References
Bai XH, Ma XL, Xu FM, Li J, Zhang H, Xiao X (2015) The drinking water treatment process as a potential source of affecting the bacterial antibiotic resistance. Sci Total Environ 533:24–31. https://doi.org/10.1016/j.scitotenv.2015.06.082
Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182. https://doi.org/10.1016/j.tim.2006.02.006
Benotti MJ, Trenholm RA, Vanderford BJ, Holady JC, Stanford BD, Snyder SA (2008) Pharmaceuticals and endocrine disrupting compounds in US drinking water. Environ Sci Technol 43:597–603
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303https://www.nature.com/articles/nmeth.f.303#supplementary-information
Chee-Sanford JC, Mackie RI, Koike S, Krapac IG, Lin YF, Yannarell AC, Maxwell S, Aminov RI (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 38:1086–1108
Chen QL, Li H, Zhou XY, Zhao Y, Su JQ, Zhang X, Huang FY (2017) An underappreciated hotspot of antibiotic resistance: the groundwater near the municipal solid waste landfill. Sci Total Environ 609:966–973. https://doi.org/10.1016/j.scitotenv.2017.07.164
Chen J, Li W, Zhang J, Qi W, Li Y, Chen S, Zhou W (2020) Prevalence of antibiotic resistance genes in drinking water and biofilms: the correlation with the microbial community and opportunistic pathogens. Chemosphere 259:127483. https://doi.org/10.1016/j.chemosphere.2020.127483
Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930. https://doi.org/10.1111/j.1654-1103.2003.tb02228.x
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Flemming HC, Percival SL, Walker JT (2002) Contamination potential of biofilms in water distribution systems. In: Malzer HJ, Gimbel R, Schippers JC (eds) Innovations in conventional and advanced water treatment processes, vol 2. Water Science and Technology: Water Supply, vol 1. Iwa Publishing, London, pp 271–280
Forsberg KJ, Patel S, Gibson MK, Lauber CL, Knight R, Fierer N, Dantas G (2014) Bacterial phylogeny structures soil resistomes across habitats. Nature 509:612–616. https://doi.org/10.1038/nature13377
Garner E, Chen C, Xia K, Bowers J, Engelthaler DM, McLain J, Edwards MA, Pruden A (2018) Metagenomic characterization of antibiotic resistance genes in full-scale reclaimed water distribution systems and corresponding potable systems. Environ Sci Technol 52:6113–6125. https://doi.org/10.1021/acs.est.7b05419
Gaze WH, Zhang L, Abdouslam NA, Hawkey PM, Calvo-Bado L, Royle J, Brown H, Davis S, Kay P, Boxall ABA, Wellington EMH (2011) Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. Isme J 5:1253–1261. https://doi.org/10.1038/ismej.2011.15
Guo XP, Li J, Yang F, Yang J, Yin DQ (2014) Prevalence of sulfonamide and tetracycline resistance genes in drinking water treatment plants in the Yangtze River Delta, China. Sci Total Environ 493:626–631. https://doi.org/10.1016/j.scitotenv.2014.06.035
Huang JJ, Hu HY, Tang F, Li Y, Lu SQ, Lu Y (2011) Inactivation and reactivation of antibiotic-resistant bacteria by chlorination in secondary effluents of a municipal wastewater treatment plant. Water Res 45:2775–2781. https://doi.org/10.1016/j.watres.2011.02.026
Jia SY, Shi P, Hu Q, Li B, Zhang T, Zhang XX (2015) Bacterial community shift drives antibiotic resistance promotion during drinking water chlorination. Environ Sci Technol 49:12271–12279. https://doi.org/10.1021/acs.est.5b03521
Khan S, Beattie TK, Knapp CW (2019) Rapid selection of antimicrobial-resistant bacteria in complex water systems by chlorine and pipe materials. Environ Chem Lett 17:1367–1373. https://doi.org/10.1007/s10311-019-00867-z
Król JE, Wojtowicz AJ, Rogers LM, Heuer H, Smalla K, Krone SM, Top EM (2013) Invasion of E. coli biofilms by antibiotic resistance plasmids. Plasmid 70:110–119. https://doi.org/10.1016/j.plasmid.2013.03.003
Lautenschlager K, Boon N, Wang YY, Egli T, Hammes F (2010) Overnight stagnation of drinking water in household taps induces microbial growth and changes in community composition. Water Res 44:4868–4877. https://doi.org/10.1016/j.watres.2010.07.032
Li B, Yang Y, Ma L, Ju F, Guo F, Tiedje JM, Zhang T (2015) Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes. ISME J 9:2490–2502. https://doi.org/10.1038/ismej.2015.59. https://www.nature.com/articles/ismej201559#supplementary-information
Li W, Wang F, Zhang J, Qiao Y, Xu C, Liu Y, Qian L, Li W, Dong B (2016) Community shift of biofilms developed in a full-scale drinking water distribution system switching from different water sources. Sci Total Environ 544:499–506. https://doi.org/10.1016/j.scitotenv.2015.11.121
Liu SS, Qu HM, Yang D, Hu H, Liu WL, Qiu ZG, Hou AM, Guo J, Li JW, Shen ZQ, Jin M (2018) Chlorine disinfection increases both intracellular and extracellular antibiotic resistance genes in a full-scale wastewater treatment plant. Water Res 136:131–136. https://doi.org/10.1016/j.watres.2018.02.036
Marshall BM, Levy SB (2011) Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev 24:718–733
McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. Isme J 6:610–618. https://doi.org/10.1038/ismej.2011.139
Ouyang WY, Huang FY, Zhao Y, Li H, Su JQ (2015) Increased levels of antibiotic resistance in urban stream of Jiulongjiang River, China. Appl Microbiol Biotechnol 99:5697–5707. https://doi.org/10.1007/s00253-015-6416-5
Pruden A, Pei RT, Storteboom H, Carlson KH (2006) Antibiotic resistance genes as emerging contaminants: Studies in northern Colorado. Environ Sci Technol 40:7445–7450. https://doi.org/10.1021/es0604131
Sanganyado E, Gwenzi W (2019) Antibiotic resistance in drinking water systems: occurrence, removal, and human health risks. Sci Total Environ 669:785–797. https://doi.org/10.1016/j.scitotenv.2019.03.162
Seiler C, Berendonk TU (2012) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol 3:10. https://doi.org/10.3389/fmicb.2012.00399
Shi P, Jia S, Zhang XX, Zhang T, Cheng S, Li A (2013) Metagenomic insights into chlorination effects on microbial antibiotic resistance in drinking water. Water Res 47:111–120. https://doi.org/10.1016/j.watres.2012.09.046
Smoot ME, Ono K, Ruscheinski J, Wang P-L, Ideker T (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27:431–432. https://doi.org/10.1093/bioinformatics/btq675
Tan QW, Li WY, Zhang JP, Zhou W, Chen JP, Li Y, Ma J (2019) Presence, dissemination and removal of antibiotic resistant bacteria and antibiotic resistance genes in urban drinking water system: a review. Front Environ Sci Eng 13:15. https://doi.org/10.1007/s11783-019-1120-9
Vu CT, Lin C, Shern CC, Yeh G, Le VG, Tran HT (2017) Contamination, ecological risk and source apportionment of heavy metals in sediments and water of a contaminated river in Taiwan. Ecol Indicatorsecol Indic 82:32–42. https://doi.org/10.1016/j.ecolind.2017.06.008
Waak MB, LaPara TM, Hallé C, Hozalski RM (2018) Occurrence of Legionella spp. in water-main biofilms from two drinking water distribution systems. Environ Sci Technol 52:7630–7639. https://doi.org/10.1021/acs.est.8b01170
Wellington EMH, Boxall ABA, Cross P, Feil EJ, Gaze WH, Hawkey PM, Johnson-Rollings AS, Jones DL, Lee NM, Otten W, Thomas CM, Williams AP (2013) The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infect Dis 13:155–165. https://doi.org/10.1016/s1473-3099(12)70317-1
Wijesiri B, Liu A, Deilami K, He B, Hong N, Yang B, Zhao X, Ayoko G, Goonetilleke A (2019) Nutrients and metals interactions between water and sediment phases: an urban river case study. Environ Pollut 251:354–362. https://doi.org/10.1016/j.envpol.2019.05.018
Witte W (1998) Medical consequences of antibiotic use in agriculture. Science 279:996–997
Xi C, Zhang Y, Marrs CF, Ye W, Simon C, Foxman B, Nriagu J (2009) Prevalence of antibiotic resistance in drinking water treatment and distribution systems. Appl Environ Microbiol 75:5714–5718
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. Environ Pollut 213:119–126. https://doi.org/10.1016/j.envpol.2016.02.013
Yang L, Hu YF, Liu Y, Zhang JD, Ulstrup J, Molin S (2011) Distinct roles of extracellular polymeric substances in Pseudomonas aeruginosa biofilm development. Environ Microbiol 13:1705–1717. https://doi.org/10.1111/j.1462-2920.2011.02503.x
Yuan QB, Zhai YF, Mao BY, Hu N (2018) Antibiotic resistance genes and intI1 prevalence in a swine wastewater treatment plant and correlation with metal resistance, bacterial community and waste. Water Parameters Ecotox Environ Saf 161:251–259. https://doi.org/10.1016/j.ecoenv.2018.05.049
Zhang ML, Chen LH, Ye CS, Yu X (2018) Co-selection of antibiotic resistance via copper shock loading on bacteria from a drinking water bio-filter. Environ Pollut 233:132–141. https://doi.org/10.1016/j.envpol.2017.09.084
Zhang ML, Wang L, Xu M, Zhou H, Wang S, Wang YJ, Bai M, Zhang C (2019) Selective antibiotic resistance genes in multiphase samples during biofilm growth in a simulated drinking water distribution system: occurrence, correlation and low-pressure ultraviolet removal. Sci Total Environ 649:146–155. https://doi.org/10.1016/j.scitotenv.2018.08.297
Zhang GS, Li WY, Chen S, Zhou W, Chen JP (2020a) Problems of conventional disinfection and new sterilization methods for antibiotic resistance control. Chemosphere 254:12. https://doi.org/10.1016/j.chemosphere.2020.126831
Zhang ML, Wan K, Zeng J, Lin WF, Ye CS, Yu X (2020b) Co-selection and stability of bacterial antibiotic resistance by arsenic pollution accidents in source water. Environ Int 135:11. https://doi.org/10.1016/j.envint.2019.105351
Zhang Y, Wang J, Lu J, Wu J (2020c) Antibiotic resistance genes might serve as new indicators for wastewater contamination of coastal waters: spatial distribution and source apportionment of antibiotic resistance genes in a coastal bay. Ecol Indicatorsecol Indic 114:106299. https://doi.org/10.1016/j.ecolind.2020.106299
Zhou S-Y-D, Zhu D, Giles M, Yang X-R, Daniell T, Neilson R, Zhu Y-G (2019) Phyllosphere of staple crops under pig manure fertilization, a reservoir of antibiotic resistance genes. Environ Pollut 252:227–235. https://doi.org/10.1016/j.envpol.2019.05.098
Zhu Y-G, Johnson TA, Su JQ, Qiao M, Guo GX, Stedtfeld RD, Hashsham SA, Tiedje JM (2013) Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci 110:3435–3440. https://doi.org/10.1073/pnas.1222743110
Zietz BP, de Vergara JD, Dunkelberg H (2003) Copper concentrations in tap water and possible effects on infant's health—results of a study in Lower Saxony, Germany. Environ Res 92:129–138. https://doi.org/10.1016/s0013-9351(03)00037-9
Funding
This work was funded by the National Natural Science Foundation of China (41807460, 41977210).
Author information
Authors and Affiliations
Contributions
F-YH and Q-LC designed the experimental protocol and carried out the experiments. XZ and S-Y-DZ assisted with the experiments. F-YH, Q-LC and S-Y-DZ wrote the manuscript. RN, J-QS revised the manuscript. All authors have read and approved the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Robert Duran
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 306 kb)
Rights and permissions
About this article
Cite this article
Huang, FY., Chen, QL., Zhang, X. et al. Dynamics of antibiotic resistance and its association with bacterial community in a drinking water treatment plant and the residential area. Environ Sci Pollut Res 28, 55690–55699 (2021). https://doi.org/10.1007/s11356-021-14896-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-14896-1