Skip to main content
Log in

Antibiotic Resistant Bacteria Found in Municipal Drinking Water

  • Original Article
  • Published:
Environmental Processes Aims and scope Submit manuscript

Abstract

Multidrug resistant bacteria in water supply systems have been emerging as a growing public health concern. Many factors affect the source and fate of these bacteria. However, conditions in the plumbing systems may contribute to the dispersion of resistance genes among bacterial populations. Through the process of lateral gene transfer, resistance genetic material can be exchanged between species in the microbial population, intensifying the problem of resistance genes. The main aim of this study was to investigate the diversity of microorganisms in tap water in Glasgow, Scotland, and the occurrence of certain antibiotic resistance genes and gene-transfer mechanisms. Results show that antibiotic resistant bacteria exist at the consumers’ end of the distribution system, some of which also contain integrase genes, which can aid in the dispersion of resistance genes. Presence of such microorganisms indicates that further investigations should be taken to assess the risks to public health.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abe Y, Skali-Lami S, Block J-C, Francius G (2012) Cohesiveness and hydrodynamic properties of young drinking water biofilms. Water Res 46(4):1155–1166. doi:10.1016/j.watres.2011.12.013

    Article  Google Scholar 

  • Ahammad ZS, Sreekrishnan TR, Hands CL, Knapp CW, Graham DW (2014) Increased waterborne blaNDM-1 resistance gene abundances associated with seasonal human pilgrimages to the upper Ganges river. Environ Sci Technol 48(5):3014–3020. doi:10.1021/es405348h

    Article  Google Scholar 

  • Allen MJ, Edberg SC, Reasoner DJ (2004) Heterotrophic plate count bacteria: what is their significance in drinking water? Int J Food Microbiol 92(3):265–274. doi:10.1016/j.ijfoodmicro.2003.08.017

    Article  Google Scholar 

  • Andersson DI, Hughes D (2010) Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol 8(4):260–271. doi:10.1038/nrmicro2319

    Google Scholar 

  • Armstrong JL, Shigeno DS, Calomiris JJ, Seidler RJ (1981) Antibiotic-resistant bacteria in drinking water. Appl Environ Microbiol 42(2):277–283

    Google Scholar 

  • Ashbolt NJ, Amezquita A, Backhaus T, Borriello P, Brandt KK, Collignon P, Anja C, Finley R, Gaze WH, Heberer T, Lawrence JR, Larsson DGJ, McEwen SA, Ryan JJ, Schonfeld J, Silley P, Snape RJ, Eede CV, Topp E (2013) Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ Health Perspect 121(9):993–1001. doi:10.1289/ehp.1206316

    Google Scholar 

  • Batt AL, Snow DD, Aga DS (2006) Occurrence of sulfonamide antimicrobials in private water wells in Washington County, Idaho, USA. Chemosphere 64(11):1963–1971. doi:10.1016/j.chemosphere.2006.01.029

    Article  Google Scholar 

  • Bjorland J, Steinum T, Sunde M, Waage S, Heir E (2003) Novel plasmid-borne gene qacJ mediates resistance to quaternary ammonium compounds in equine Staphylococcus aureus, Staphylococcus simulans, and Staphylococcus intermedius. Antimicrob Agents Chemother 47(10):3046–3052. doi:10.1128/AAC.47.10.3046-3052.2003

    Article  Google Scholar 

  • Boucher Y, Labbate M, Koenig JE, Stokes HW (2007) Integrons: mobilizable platforms that promote genetic diversity in bacteria. Trends Microbiol 15(7):301–309. doi:10.1016/j.tim.2007.05.004

    Article  Google Scholar 

  • Bridier A, Briandet R, Thoma V, Dubios-Brissonnet F (2011) Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27(9):1017–1032. doi:10.1080/08927014.2011.626899

    Article  Google Scholar 

  • Brunkard JM, Ailes E, Roberts VA, Hill V, Hilborn ED, Craun GF, Rajasingham A, Kahler A, Garrison L, Hicks L, Carpenter J, Wade TJ, Beach MJ, Yoder JS (2011) Surveillance for waterborne disease outbreaks associated with drinking water. United States, 2007–2008. Morbity Mortal. Weekly Rep 60 (ss12), 38–68.

  • Buffet-Bataillon S, Tattevin P, Bonnaure-Mallet M, Jolivet-Gougeon A (2012) Emergence of resistance to antibacterial agents: the role of quaternary ammonium compounds-a critical review. Int J Antimicrob Agents 39(5):381–389. doi:10.1016/j.ijantimicag.2012.01.011

    Article  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S-rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108(Suppl 1):4516–4522. doi:10.1073/pnas.1000080107

    Article  Google Scholar 

  • CDC (2013) Antibiotic resistance threats in the United States, 2013. Center for Disease Control and Prevention, U. S. Department of Health and Human Servises, USA, pp 1–114

    Google Scholar 

  • Chakravorty S, Helb D, Burday M, Connell N, Alland D (2007) A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. J Microbiol Methods 69(2):330–339. doi:10.1016/j.mimet.2007.02.005

    Article  Google Scholar 

  • Chapman JS (2003) Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int Biodeterior Biodegrad 51(4):271–276. doi:10.1016/s0964-8305(03)00044-1

    Article  Google Scholar 

  • Chen J, Liu YS, Su HC, Ying GG, Liu F, Liu SS, He LY, Chen ZF, Yang YQ, Chen FR (2015a) Removal of antibiotics and antibiotic resistance genes in rural wastewater by an integrated constructed wetland. Environ Sci Pollut Res Int 22:1794–1803. doi:10.1007/s11356-014-2800-4

    Article  Google Scholar 

  • Chen B, Liang X, Nie X, Huang X, Zou S, Li X (2015b) The role of class I integrons in the dissemination of sulfonamide resistance genes in the Pearl River and Pearl River Estuary, South China. J Hazard Mater 282:61–67. doi:10.1016/j.jhazmat.2014.06.010

    Article  Google Scholar 

  • Chiao T-H, Clancy TM, Pinto A, Xi C, Raskin L (2014) Differential resistance of drinking water bacteial populations to monochloriamine disinfection. Environ Sci Technol 48:4038–4047. doi:10.1021/es4055725

    Article  Google Scholar 

  • Demarre G, Frumerie C, Gopaul DN, Mazel D (2007) Identification of key structural determinants of the IntI1 integron integrase that influence attC x attI1 recombination efficiency. Nucleic Acids Res 35(19):6475–6489. doi:10.1093/nar/gkm709

    Article  Google Scholar 

  • Drancourt M, Bollet C, Carlioz A, Martelin R, Gayral J-P, Raoult D (2000) 16S ribosomal DNA sequence analysis of a large collection of environmental and clinical unidentifiable bacterial isolates. J Clin Microbiol 38(10):3623–3630

    Google Scholar 

  • Enne VI, Bennett PM, Livermore DM, Hall LM (2004) Enhancement of host fitness by the sul2-coding plasmid p9123 in the absence of selective pressure. J Antimicrob Chemother 53(6):958–963. doi:10.1093/jac/dkh217

    Article  Google Scholar 

  • Fick J, Soderstrom H, Lindberg RH, Phan C, Tysklind M, Larsson DGJ (2009) Contamination of surface, ground and drinking water from pharmateutical production. Environ Toxicol Chem 28(12):2522–2527. doi:10.1897/09-073.S1

    Article  Google Scholar 

  • Gallego V, Garcia MT, Ventosa A (2005) Methylobacterium hispanicum sp. nov. and Methylobacterium aquaticum sp. nov., isolated from drinking water. Int J Syst Evol Microbiol 55(Pt 1):281–287. doi:10.1099/ijs.0.63319-0

    Article  Google Scholar 

  • Gaze WH, Abdouslam N, Hawkey PM, Wellington EM (2005) Incidence of class 1 integrons in a quaternary ammonium compound-polluted environment. Antimicrob Agents Chemother 49(5):1802–1807. doi:10.1128/AAC.49.5.1802-1807.2005

    Article  Google Scholar 

  • Gaze WH, Zhang L, Abdouslam NA, Hawkey PM, Calvo-Bado L, Royle J, Brown H, Davis S, Kay P, Boxall AB, Wellington EM (2011) Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J 5(8):1253–1261. doi:10.1038/ismej.2011.15

    Article  Google Scholar 

  • Gillings M, Boucher Y, Labbate M, Holmes A, Krishnan S, Holley M, Stokes HW (2008) The evolution of class 1 integrons and the rise of antibiotic resistance. J Bacteriol 190(14):5095–5100. doi:10.1128/JB.00152-08

    Article  Google Scholar 

  • Gillings MR, Xuejun D, Hardwick SA, Holley MP, Stokes HW (2009) Gene cassettes encoding resistance to quaternary ammonium compounds: a role in the origin of clinical class 1 integrons? ISME J 3(2):209–215. doi:10.1038/ismej.2008.98

    Article  Google Scholar 

  • Gundogdu A, Long YB, Vollmerhausen TL, Katouli M (2011) Antimicrobial resistance and distribution of sul genes and integron-associated intI genes among uropathogenic Escherichia coli in Queensland, Australia. J Med Microbiol 60(Pt 11):1633–1642. doi:10.1099/jmm.0.034140-0

    Article  Google Scholar 

  • Hartmann J, Beyer R, Harm S (2014) Effective removal of estrogens from drinking water and wastewater by adsorption technology. Environ Process 1:87–94. doi:10.1007/s40710-014-0005-y

    Article  Google Scholar 

  • Hong PY, Hwang C, Ling F, Andersen GL, LeChevallier MW, Liu WT (2010) Pyrosequencing analysis of bacterial biofilm communities in water meters of a drinking water distribution system. Appl Environ Microbiol 76(16):5631–5635. doi:10.1128/AEM.00281-10

    Article  Google Scholar 

  • Howard K, Inglis TJJ (2003) The effect of free chlorine on Burkholderia pseudomallei in potable water. Water Res 37:4425–4432. doi:10.1016/S0043-1354(03)00440-8

    Article  Google Scholar 

  • Jaglic Z, Cervinkova D (2012) Genetic basis of resistance to quaternary ammonium compounds - the qac genes and their role: a review. Vet Med 57(6):275–281

    Google Scholar 

  • Janda JM, Abbott SL (2007) 16S-rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol 45(9):2761–2764. doi:10.1128/JCM.01228-07

    Article  Google Scholar 

  • Jechalke S, Schreiter S, Wolters B, Dealtry S, Heuer H, Smalla K (2013) Widespread dissemination of class 1 integron components in soils and related ecosystems as revealed by cultivation-independent analysis. Front Microbiol 4:420–427. doi:10.3389/fmicb.2013.00420

    Google Scholar 

  • Jeong JH, Shin KS, Lee JW, Park EJ, Son SY (2009) Analysis of a novel class 1 integron containing metallo-beta-lactamase gene VIM-2 in Pseudomonas aeruginosa. J Microbiol 47(6):753–759. doi:10.1007/s12275-008-0272-2

    Article  Google Scholar 

  • Khan GA, Berglund B, Khan KM, Lindgren PE, Fick J (2013) Occurrence and abundance of antibiotics and resistance genes in rivers, canal and near drug formulation facilities-a study in Pakistan. PLoS One 8(6), e62712. doi:10.1371/journal.pone.0062712

    Article  Google Scholar 

  • Khan S, Beattie TK, Knapp CW (2016) Relationship between antibiotic- and disinfectant-resistant profiles in bacteria harvested from tap water. Chemosphere 152:132-141. doi:10.1016/j.chemosphere.2016.02.086.

  • Kilvington S, Gray T, Dart J, Morlet N, Beeching JR, Frazer DG, Matheson M (2004) Acanthamoeba Keratitis: The role of domestic tap water contamination in the United Kingdom. Invest Ophthalmol Vis Sci 45(1):165–169. doi:10.1167/iovs.03-0559

    Article  Google Scholar 

  • Kucken D, Feucht H-H, Kaulfers P-M (2000) Association of qacE and qacE1 with muptiple resistance to antibiotics and antiseptics in clinical isolates of Gram-negative bacteria. FEMS Microbiol Lett 183:95–98. doi:10.1111/j.1574-6968.2000.tb08939.x

    Article  Google Scholar 

  • Kumar S, Tripathi VR, Garg SK (2013) Antibiotic resistance and genetic diversity in water-borne Enterobacteriaceae isolates from recreational and drinking water sources. Int J Environ Sci Technol 10:789–798. doi:10.1007/s13762-012-0126-7

    Article  Google Scholar 

  • Larsson DGJ, Pedro CD, Paxeus N (2007) Effluent from drug manufacturers contains extremely high levels of pharmaceuticals. J Hazard Mater 148:751–755. doi:10.1016/j.jhazmat.2007.07.008

    Article  Google Scholar 

  • LeChevallier MW, Hassenauer TS, Camper AK, McFeters GA (1984) Disinfection of bacteria attached to granular activated carbon. Appl Environ Microbiol 48(5):918–923

    Google Scholar 

  • LeChevallier MW, Cawthon CD, Lee RG (1988) Factors promoting survival of bacteria in chlorinated water supplies. Appl Environ Microbiol 53(4):649–654

    Google Scholar 

  • Lee J, Lee CS, Hugunin KM, Maute CJ, Dysko RC (2010) Bacteria from drinking water supply and their fate in gastrointestinal tracts of germ-free mice: a phylogenetic comparison study. Water Res 44(17):5050–5058. doi:10.1016/j.watres.2010.07.027

    Article  Google Scholar 

  • Levy SB (2002) Factors impacting on the problem of antibiotic resistance. J Antimicrob Chemother 49:25–30

    Article  Google Scholar 

  • Luo Y, Mao D, Rysz M, Zhou Q, Zhang H, Xu L, Alvarez PJJ (2010) Trends in antibiotic resistance genes occurrence in the Haihe River, China. Environ Sci Technol 44(19):7220–7225. doi:10.1021/es100233w

    Article  Google Scholar 

  • Mazel D (2006) Integrons: agents of bacterial evolution. Nat Rev Microbiol 4(8):608–620. doi:10.1038/nrmicro1462

    Article  Google Scholar 

  • Mignard S, Flandrois JP (2006) 16S-rRNA sequencing in routine bacterial identification: a 30-month experiment. J Microbiol Methods 67(3):574–581. doi:10.1016/j.mimet.2006.05.009

    Article  Google Scholar 

  • Mokracka J, Koczura R, Kaznowski A (2012) Multiresistant Enterobacteriaceae with class 1 and class 2 integrons in a municipal wastewater treatment plant. Water Res 46(10):3353–3363. doi:10.1016/j.watres.2012.03.037

    Article  Google Scholar 

  • Molin S, Tolker-Nielsen T (2003) Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 14(3):255–261. doi:10.1016/s0958-1669(03)00036-3

    Article  Google Scholar 

  • Morente OE, Fernandez-Fuentes MA, Grande Burgos MJ, Abriouel H, Perez Pulido R, Galvez A (2013) Biocide tolerance in bacteria. Int J Food Microbiol 162(1):13–25. doi:10.1016/j.ijfoodmicro.2012.12.028

    Article  Google Scholar 

  • Norton CD, LeChevallier MW (2000) A pilot study of bacteriological population changes through potable water treatment and distribution. Appl Environ Microbiol 66(1):268–276

    Article  Google Scholar 

  • Paulsen IT, Littlejohn TG, Rådström P, Sundström L, Sköld O, Swedberg G, Skurray RA (1993) The 3′ conserved segment of integrons contains a gene associated with multidrug resistance to antiseptics and disinfectants. Antimicrob Agents Chemother 37(4):761–768. doi:10.1128/AAC.37.4.761

    Article  Google Scholar 

  • Paulsen IT, Brown MH, Littlejohn TG, Michell BA, Skurry RA (1996) Multidrug resistance proteins QacA and QacB from Staphylococcus aureus: Membrane topology and identification of residues involved in substrate specificity. Proc Natl Acad Sci U S A 93:3630–3635

    Article  Google Scholar 

  • Pei R, Kim S-C, Carlson KH, Pruden A (2006) Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res 40(12):2427–2435. doi:10.1016/j.watres.2006.04.017

    Article  Google Scholar 

  • Pruden A, Pei R, Storteboom H, Carlson KH (2006) Antibiotic resistance genes as emerging contaminants: Studies in Northern Colorado. Environ Sci Technol 40(23):7445–7450.

    Article  Google Scholar 

  • Pruden A, Arabi M, Storteboom HN (2012) Correlation between upstream human activities and riverine antibiotic resistance genes. Environ Sci Technol 46(21):11541–11549. doi:10.1021/es302657r

    Article  Google Scholar 

  • Pruden A, Larsson DGJ, Amezquita A, Collignon P, Brandt KK, Graham DW, Lazorchak JM, Suzuki S, Silley P, Snape JR, Topp E, Zhang T, Zhu Y-G (2013) Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environ Health Perspect 121(8):878–886. doi:10.1289/ehp.1206446

    Article  Google Scholar 

  • Ribeiro AF, Bodilis J, Alonso L, Buquet S, Feuilloley M, Dupont J-P, Pawlak B (2014) Occurrence of multi-antibiotic resistant Pseudomonas spp. in drinking water produced from karstic hydrosystems. Sci Total Environ 490:370–378. doi:10.1016/j.scitotenv.2014.05.012

    Article  Google Scholar 

  • Ridgway HF, Olson BH (1982) Chlorine resistance patterns of bacteria from two drinking water distribution systems. Appl Environ Microbiol 44(4):972–987

    Google Scholar 

  • Shearer JE, Summers AO (2009) Intracellular steady-state concentration of integron recombination products varies with integrase level and growth phase. J Mol Biol 386(2):316–331. doi:10.1016/j.jmb.2008.12.041

    Article  Google Scholar 

  • 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(1):111–120. doi:10.1016/j.watres.2012.09.046

    Article  Google Scholar 

  • Simoes LC, Simoes M, Vieira MJ (2010) Influence of the diversity of bacterial isolates from drinking water on resistance of biofilms to disinfection. Appl Environ Microbiol 78(19):6673–6679. doi:10.1128/AEM.00872-10

    Article  Google Scholar 

  • Stalder T, Barraud O, Casellas M, Dagot C, Ploy MC (2012) Integron involvement in environmental spread of antibiotic resistance. Front Microbiol 3:119–132. doi:10.3389/fmicb.2012.00119

    Article  Google Scholar 

  • Stokes HW, Gillings MR (2011) Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS Microbiol Rev 35(5):790–819. doi:10.1111/j.1574-6976.2011.00273.x

    Article  Google Scholar 

  • Stokes HW, Hall RM (1989) A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: integrons. Mol Microbiol 3(12):1669–1683

    Article  Google Scholar 

  • Stoll C, Sidhu JP, Tiehm A, Toze S (2012) Prevalence of clinically relevant antibiotic resistance genes in surface water samples collected from Germany and Australia. Environ Sci Technol 46(17):9716–9726. doi:10.1021/es302020s

    Article  Google Scholar 

  • Tenover FC (2006) Mechanisms of antimicrobial resistance in bacteria. Am J Med 119(6A):S3–S10. doi:10.1016/j.amjmed.2006.03.011

    Article  Google Scholar 

  • Vaz-Moreira I, Nunes OC, Manaia CM (2012) Diversity and antibiotic resistance in Pseudomonas spp. from drinking water. Sci Total Environ 426:366–374. doi:10.1016/j.scitotenv.2012.03.046

    Article  Google Scholar 

  • Wang H, Edwards MA, Falkinham JO 3rd, Pruden A (2013) Probiotic approach to pathogen control in premise plumbing systems? A Review. Environ Sci Technol 47:10117–10128. doi:10.1021/es402455r

    Article  Google Scholar 

  • Wingender J, Flemming HC (2011) Biofilms in drinking water and their role as reservoir for pathogens. Int J Hyg Environ Health 214(6):417–423. doi:10.1016/j.ijheh.2011.05.009

    Article  Google Scholar 

  • Woo PCY, Ng KHL, Lau SKP, Yip K, Fung AMY, Kw L et al (2003) Usefulness of the MicroSeq 500 16S Ribosomal DNA-Based bacterial identification system for identification of clinically significant bacterial isolates with ambiguous biochemical profiles. J Clin Microbiol 41(5):1996–2001. doi:10.1128/jcm.41.5.1996-2001.2003

    Article  Google Scholar 

  • 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(17):5714–5718. doi:10.1128/AEM.00382-09

    Article  Google Scholar 

  • Xu W, Zhang G, Li X, Zou S, Li P, Hu Z, Li J (2007) Occurrence and elimination of antibiotics at four sewage treatment plants in the Pearl River Delta (PRD), South China. Water Res 41(19):4526–4534. doi:10.1016/j.watres.2007.06.023

    Article  Google Scholar 

  • Xu Z, Li L, Shirtliff ME, Peters BM, Li B, Peng Y, Alam MJ, Yamasaki S, Shi L (2011) Resistance class 1 integron in clinical methicillin-resistant Staphylococcus aureus strains in southern China, 2001–2006. Clin Microbiol Infect 17(5):714–718. doi:10.1111/j.1469-0691.2010.03379.x

    Article  Google Scholar 

Download references

Acknowledgments

PhD work of SK is supported by the “Faculty for the Future” grant scheme from Schlumberger Foundation.

An initial version of this paper has been presented at the 9th World Congress of the European Water Resources Association (EWRA) “Water Resources Management in a Changing World: Challenges and Opportunities”, Istanbul, Turkey, June 10–13, 2015.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sadia Khan.

Ethics declarations

Conflict of Interest

No conflict of interest is found.

Additional information

Highlights

• Plumbing systems contain antibiotic resistance bacteria

sul1 and sul2 genes are found in bacteria which show resistance against sulfonamides drugs

• The presence of integrons suggests that resistance traits can be transferred to other bacteria

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, S., Knapp, C.W. & Beattie, T.K. Antibiotic Resistant Bacteria Found in Municipal Drinking Water. Environ. Process. 3, 541–552 (2016). https://doi.org/10.1007/s40710-016-0149-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40710-016-0149-z

Keywords

Navigation