Effect of ultraviolet irradiation and chlorination on ampicillin-resistant Escherichia coli and its ampicillin resistance gene

Abstract

Antibiotic resistance is a serious public health risk that may spread via potable and reclaimed water. Effective disinfection is important for inactivation of antibiotic-resistant bacteria and disruption of antibiotic resistance genes. Ampicillin is a widely prescribed antibiotic but its effectiveness is increasingly undermined by resistance. In this study, changes in ampicillin resistance for Escherichia coli (E. coli) CGMCC 1.1595 were analyzed after exposure to different doses of ultraviolet (UV) or chlorine, and damage incurred by the plasmid encoding ampicillin resistance gene bla_TEM-1 was assessed. We reported a greater stability in ampicillin-resistant E. coli CGMCC 1.1595 after UV irradiation or chlorination when compared with previously published data for other E. coli strains. UV irradiation and chlorination led to a shift in the mortality frequency distributions of ampicillin-resistant E. coli when subsequently exposed to ampicillin. The ampicillin hemi-inhibitory concentration (IC₅₀) without disinfection was 3800 mg·L^-1, and an increment was observed after UV irradiation or chlorination. The IC₅₀ of ampicillin-resistant E. coli was 1.5-fold higher at a UV dose of 40 mJ·cm^-2, and was 1.4-fold higher when exposed to 2.0 mg·L^-1 chlorine. These results indicate that UV irradiation and chlorination can potentially increase the risk of selection for E. coli strains with high ampicillin resistance. There was no evident damage to bla_TEM-1 after 1–10 mg Cl₂·L^-1 chlorination, while a UV dose of 80 mJ·cm^-2 yielded a damage ratio for bla_TEM-1 of approximately 1.2-log. Therefore, high UV doses are required for effective disruption of antibiotic resistance genes in bacteria.

Keywords

antibiotic resistance / Escherichia coli / ampicillin resistance gene / ultraviolet irradiation / chlorination

References

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

[2] Shah S Q A, Colquhoun D J, Nikuli H L, Sørum H. Prevalence of antibiotic resistance genes in the bacterial flora of integrated fish farming environments of Pakistan and Tanzania. Environmental Science & Technology, 2012, 46(16): 8672–8679

[3] Chee-Sanford J C, Aminov R I, Krapac I J, Garrigues-Jeanjean N, Mackie R I. Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Applied and Environmental Microbiology, 2001, 67(4): 1494–1502

[4] Storteboom H, Arabi M, Davis J G, Crimi B, Pruden A. Identification of antibiotic-resistance-gene molecular signatures suitable as tracers of pristine river, urban, and agricultural sources. Environmental Science & Technology, 2010, 44(6): 1947–1953

[5] Schwartz T, Kohnen W, Jansen B, Obst U. Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiology Ecology, 2003, 43(3): 325–335

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

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

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

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

[10] Rizzo L, Manaia C, Merlin C, Schwartz T, Dagot C, Ploy M C, Michael I, Fatta-Kassinos D. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: a review. Science of the Total Environment, 2013, 447: 345–360

[11] Huang J J, Hu H Y, Lu S Q, Li Y, Tang F, Lu Y, Wei B. Monitoring and evaluation of antibiotic-resistant bacteria at a municipal wastewater treatment plant in China. Environment International, 2012, 42: 31–36

[12] Zhang T, Zhang X X, Ye L. Plasmid metagenome reveals high levels of antibiotic resistance genes and mobile genetic elements in activated sludge. PLoS ONE, 2011, 6(10): e26041

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

[14] Meckes M C. Effect of UV light disinfection on antibiotic-resistant coliforms in wastewater effluents. Applied and Environmental Microbiology, 1982, 43(2): 371–377

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

[16] Livermore D M, Yuan M. Antibiotic resistance and production of extended-spectrum beta-lactamases amongst Klebsiella spp. from intensive care units in Europe. The Journal of Antimicrobial Chemotherapy, 1996, 38(3): 409–424

[17] Malouin F, Bryan L E. Modification of penicillin-binding proteins as mechanisms of beta-lactam resistance. Antimicrobial Agents and Chemotherapy, 1986, 30(1): 1–5

[18] Volkmann H, Schwartz T, Bischoff P, Kirchen S, Obst U. Detection of clinically relevant antibiotic-resistance genes in municipal wastewater using real-time PCR (TaqMan). Journal of Microbiological Methods, 2004, 56(2): 277–286

[19] Sutcliffe J G. Nucleotide-sequence of the ampicillin resistance gene of Escherichia-coli plasmid pBR322. Proceedings of the National Academy of Sciences of the United States of America, 1978, 75(8): 3737–3741

[20] Bolton J R, Linden K G. Standardization of methods for fluence (UV dose) determination in bench-scale UV experiments. Journal of Environmental Engineering, 2003, 129(3): 209–215

[21] Guo M T, Hu H Y, Bolton J R, El-Din M G. Comparison of low- and medium-pressure ultraviolet lamps: photoreactivation of Escherichia coli and total coliforms in secondary effluents of municipal wastewater treatment plants. Water Research, 2009, 43(3): 815–821

[22] Hijnen W A M, Beerendonk E F, Medema G J. Inactivation credit of UV radiation for viruses, bacteria and protozoan (oo)cysts in water: a review. Water Research, 2006, 40(1): 3–22

[23] Stewart M A, Olson B H. Bacterial Resistance to Potable Water Disinfectant. Cambridge: Cambridge University Press, 1996, 140–192

[24] Armstrong J L, Shigeno D S, Calomiris J J, Seidler R J. Antibiotic-resistant bacteria in drinking water. Applied and Environmental Microbiology, 1981, 42(2): 277–283

[25] Li X Z, Mehrotra M, Ghimire S, Adewoye L. β-Lactam resistance and β-lactamases in bacteria of animal origin. Veterinary Microbiology, 2007, 121(3-4): 197–214

[26] Kim S, Park H, Chandran K. Propensity of activated sludge to amplify or attenuate tetracycline resistance genes and tetracycline resistant bacteria: a mathematical modeling approach. Chemosphere, 2010, 78(9): 1071–1077

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

[28] Speer B S, Shoemaker N B, Salyers A A. Bacterial resistance to tetracycline: mechanisms, transfer, and clinical significance. Clinical Microbiology Reviews, 1992, 5(4): 387–399

[29] Chopra I, Roberts M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiology and Molecular Biology Reviews, 2001, 65(2): 232–260

[30] Guo M, Huang J, Hu H, Liu W, Yang J. UV inactivation and characteristics after photoreactivation of Escherichia coli with plasmid: health safety concern about UV disinfection. Water Research, 2012, 46(13): 4031–4036

[31] Courcelle J, Donaldson J R, Chow K H, Courcelle C T. DNA damage-induced replication fork regression and processing in Escherichia coli. Science, 2003, 299(5609): 1064–1067

[32] Munakata N, Ikeda Y. Inactivation of transforming DNA by ultraviolet irradiation-A study with ultraviolet-sensitive mutants of Bacillus subtilis. Mutation Research, 1969, 7(2): 133–139

Acknowledgements

The author thanks the National Natural Science Foundation of China (Key Project, Grant No. 51138006) and State Key Joint Laboratory of Environment Simulation and Pollution Control (Project, No. 13L01ESPC) for financial support. The research is also supported by the Collaborative Innovation Center for Regional Environmental Quality.

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg