Inactivation of Antibiotic Resistant Bacteria and Resistance Genes by Ozone: From Laboratory Experiments to Full-Scale Wastewater Treatment

Environmental Science and Technology

Volumn 50, Issue 21, 2016, Pages 11862-11871

  Czekalski, Nadine ^a   Imminger, Stefanie ^a   Salhi, Elisabeth ^a   Veljkovic, Marjan ^a   Kleffel, Karolin ^a   Drissner, David ^b   Hammes, Frederik ^a   Bürgmann, Helmut ^a   Von Gunten, Urs ^a,c,d  

^a SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

^b AGROSCOPE   (Switzerland)

^c ETH ZURICH   (Switzerland)

^d EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BACTERIA; ESCHERICHIA COLI; GENES; OZONE; OZONE RESISTANCE; OZONIZATION; PLANTS (BOTANY); POLYMERASE CHAIN REACTION; SULFUR COMPOUNDS; WASTEWATER TREATMENT; WATER TREATMENT;

ANTIBIOTIC RESISTANCE GENES; ANTIBIOTIC-RESISTANT BACTERIA; BACTERIAL INACTIVATION; FULL-SCALE APPLICATIONS; FUTURE CHALLENGES; LABORATORY EXPERIMENTS; QUANTITATIVE REAL TIME PCR; WASTEWATER TREATMENT PLANTS;

OZONE WATER TREATMENT;

OZONE; RNA 16S; SULFANILAMIDE; ANTIINFECTIVE AGENT; WASTE WATER;

ANTIBIOTIC RESISTANCE; COLIFORM BACTERIUM; EXPERIMENTAL STUDY; FLOW CYTOMETRY; GENETIC ANALYSIS; LABORATORY METHOD; MEMBRANE; OZONATION; REACTION KINETICS; WASTEWATER TREATMENT PLANT;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENE; ARTICLE; BACTERIAL GENE; DOSE RESPONSE; ESCHERICHIA COLI; FLOW CYTOMETRY; GENE DISRUPTION; GENE DOSAGE; NONHUMAN; OXIDATIVE STRESS; OZONATION; PH; PLASMID; PLATE COUNT; QUANTITATIVE ASSAY; REAL TIME POLYMERASE CHAIN REACTION; WASTE WATER MANAGEMENT; WATER POLLUTANT; BACTERIUM; DRUG EFFECTS; MICROBIOLOGY; SEWAGE; WASTE WATER; WATER MANAGEMENT;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ANTI-BACTERIAL AGENTS; BACTERIA; ESCHERICHIA COLI; OZONE; WASTE DISPOSAL, FLUID; WASTE WATER; WATER PURIFICATION;

EID: 84994301925     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.6b02640     Document Type: Article

References (68)

1. Sumpter, J. P.; Johnson, A. C. 10th Anniversary Perspective: Reflections on endocrine disruption in the aquatic environment: from known knowns to unknown unknowns (and many things in between) J. Environ. Monit. 2008, 10 (12) 1476-1485 10.1039/b815741n
2. Schwarzenbach, R. P.; Escher, B. I.; Fenner, K.; Hofstetter, T. B.; Johnson, C. A.; von Gunten, U.; Wehrli, B. The challenge of micropollutants in aquatic systems Science 2006, 313 (5790) 1072-1077 10.1126/science.1127291
3. Antimicrobial Resistance: Global Report on Surveillance 2014; WHO World Health Organisation: Geneva, April 2014; http://apps.who.int/iris/bitstream/10665/112642/1/9789241564748-eng.pdf?ua=1.
4. Berendonk, T. U.; Manaia, C. M.; Merlin, C.; Fatta-Kassinos, D.; Cytryn, E.; Walsh, F.; Burgmann, H.; Sorum, H.; Norstrom, M.; Pons, M.-N.; Kreuzinger, N.; Huovinen, P.; Stefani, S.; Schwartz, T.; Kisand, V.; Baquero, F.; Martinez, J. L. Tackling antibiotic resistance: the environmental framework Nat. Rev. Microbiol. 2015, 13 (5) 310-317 10.1038/nrmicro3439
5. Pruden, A.; Pei, R.; Storteboom, H.; Carlson, K. H. Antibiotic resistance genes as emerging contaminants: Studies in Northern Colorado Environ. Sci. Technol. 2006, 40 (23) 7445-7450 10.1021/es060413l
6. Gatica, J.; Cytryn, E. Impact of treated wastewater irrigation on antibiotic resistance in the soil microbiome Environ. Sci. Pollut. Res. 2013, 20 (6) 3529-3538 10.1007/s11356-013-1505-4
7. Czekalski, N.; Sigdel, R.; Birtel, J.; Matthews, B.; Bürgmann, H. Does human activity impact the natural antibiotic resistance background? Abundance of antibiotic resistance genes in 21 Swiss lakes Environ. Int. 2015, 81, 45-55 10.1016/j.envint.2015.04.005
8. Czekalski, N.; Gascon Diez, E.; Bürgmann, H. Wastewater as a point source of antibiotic-resistance genes in the sediment of a freshwater lake ISME J. 2014, 8, 1381 10.1038/ismej.2014.8
9. 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 Sci. Total Environ. 2013, 447 (0) 345-360 10.1016/j.scitotenv.2013.01.032
10. Czekalski, N.; Berthold, T.; Caucci, S.; Egli, A.; Bürgmann, H. Increased levels of multiresistant bacteria and resistance genes after wastewater treatment and their dissemination into Lake Geneva, Switzerland Front. Microbiol. 2012, 10.3389/fmicb.2012.00106
11. Ternes, T.; Joss, A. Human Pharmaceuticals, Hormones and Fragrances The Challenge of micropollutants in urban water management; IWA Publishing: London, 2007.
12. Gewässerschutzverordnung (GschV) vom 28. Oktober 1998 (Stand am 2. Februar 2016). SR 814.201, 2016. https://www.admin.ch/opc/de/classified-compilation/19983281/201602020000/814.201.pdf.
13. The Swiss Federal Council. Waters protection Ordinance (WPO). https://www.admin.ch/opc/en/classified-compilation/19983281/index.html (accessed 26.09. 2016).
14. Eggen, R. I. L.; Hollender, J.; Joss, A.; Scharer, M.; Stamm, C. Reducing the discharge of micropollutants in the aquatic environment: The benefits of upgrading wastewater treatment plants Environ. Sci. Technol. 2014, 48 (14) 7683-7689 10.1021/es500907n
15. Gerrity, D.; Gamage, S.; Jones, D.; Korshin, G. V.; Lee, Y.; Pisarenko, A.; Trenholm, R. A.; von Gunten, U.; Wert, E. C.; Snyder, S. A. Development of surrogate correlation models to predict trace organic contaminant oxidation and microbial inactivation during ozonation Water Res. 2012, 46 (19) 6257-6272 10.1016/j.watres.2012.08.037
16. Lee, Y.; Gerrity, D.; Lee, M.; Bogeat, A. E.; Salhi, E.; Gamage, S.; Trenholm, R. A.; Wert, E. C.; Snyder, S. A.; von Gunten, U. Prediction of micropollutant elimination during ozonation of municipal wastewater effluents: Use of kinetic and water specific information Environ. Sci. Technol. 2013, 47 (11) 5872-5881 10.1021/es400781r
17. von Gunten, U. Ozonation of drinking water: Part II. Disinfection and by-product formation in presence of bromide, iodide or chlorine Water Res. 2003, 37 (7) 1469-1487 10.1016/S0043-1354(02)00458-X
18. von Sonntag, C.; von Gunten, U. Chemistry of Ozone in Water and Wastewater Treatment from Basic Principles to Applications; IWA Publishing: London, 2012.
19. Hamelin, C.; Chung, Y. S. Optimal conditions for mutagenesis by ozone in Escherichia coli K12 Mutat. Res., Fundam. Mol. Mech. Mutagen. 1974, 24 (3) 271-279 10.1016/0027-5107(74)90175-4
20. Ishizaki, K.; Sawadaishi, K.; Miura, K.; Shinriki, N. Effect of ozone on plasmid DNA of Escherichia coli in situ Water Res. 1987, 21 (7) 823-827 10.1016/0043-1354(87)90158-8
21. Hamelin, C.; Sarhan, F.; Chung, Y. S. Induction of deoxyribonucleic acid degradation in Escherichia coli by ozone Experientia 1978, 34 (12) 1578-1579 10.1007/BF02034684
22. Hamelin, C.; Sarhan, F.; Chung, Y. S. Ozone induced DNA degradation in different DNA polymerase I mutants of Escherichia coli K12 Biochem. Biophys. Res. Commun. 1977, 77 (1) 220-224 10.1016/S0006-291X(77)80185-X
23. Dodd, M. C. Potential impacts of disinfection processes on elimination and deactivation of antibiotic resistance genes during water and wastewater treatment J. Environ. Monit. 2012, 14, 1754 10.1039/c2em00006g
24. Scott, D. B. M.; Lesher, E. C. Effect of ozone on survival and permeability of Escherichia coli J. Bacteriol. 1963, 85 (3) 567-576
25. Hunt, N. K.; Mariñas, B. J. Inactivation of Escherichia coli with ozone: chemical and inactivation kinetics Water Res. 1999, 33 (11) 2633-2641 10.1016/S0043-1354(99)00115-3
26. Casolari, A., Microbial Death. In Physiological Models in Microbiology; Bazin, M. J.; Prosser, J. I., Eds.; CRC Press: Boca Raton, FL, 1988; Vol. II, pp 1-44.
27. Broadwater, W. T.; Hoehn, R. C.; King, P. H. Sensitivity of three selected bacterial species to ozone Appl. Microbiol. 1973, 26 (3) 391-393
28. Patil, S.; Valdramidis, V. P.; Karatzas, K. A. G.; Cullen, P. J.; Bourke, P. Assessing the microbial oxidative stress mechanism of ozone treatment through the responses of Escherichia coli mutants J. Appl. Microbiol. 2011, 111 (1) 136-144 10.1111/j.1365-2672.2011.05021.x
29. Xu, P.; Janex, M.-L.; Savoye, P.; Cockx, A.; Lazarova, V. Wastewater disinfection by ozone: main parameters for process design Water Res. 2002, 36 (4) 1043-1055 10.1016/S0043-1354(01)00298-6
30. Patil, S.; Bourke, P.; Frias, J. M.; Tiwari, B. K.; Cullen, P. J. Inactivation of Escherichia coli in orange juice using ozone Innovative Food Sci. Emerging Technol. 2009, 10 (4) 551-557 10.1016/j.ifset.2009.05.011
31. Tang, K. W.; Dziallas, C.; Grossart, H.-P. Zooplankton and aggregates as refuge for aquatic bacteria: protection from UV, heat and ozone stresses used for water treatment Environ. Microbiol. 2011, 13 (2) 378-390 10.1111/j.1462-2920.2010.02335.x
32. Pak, G.; Salcedo, D. E.; Lee, H.; Oh, J.; Maeng, S. K.; Song, K. G.; Hong, S. W.; Kim, H.-C.; Chandran, K.; Kim, S. Comparison of antibiotic resistance removal efficiencies using ozone disinfection under different pH and suspended solids and humic substance concentrations Environ. Sci. Technol. 2016, 50 (14) 7590-7600 10.1021/acs.est.6b01340
33. Hamelin, C.; Sup Chung, Y. Repair of ozone-induced DNA lesions in Escherichia coli B cells Mutat. Res., Fundam. Mol. Mech. Mutagen. 1989, 214 (2) 253-255 10.1016/0027-5107(89)90169-3
34. Jiménez-Arribas, G.; Léautaud, V.; Amábile-Cuevas, C. F. Regulatory locus soxRS partially protects Escherichia coli against ozone FEMS Microbiol. Lett. 2001, 195 (2) 175-177 10.1111/j.1574-6968.2001.tb10517.x
35. Alexander, J.; Knopp, G.; Dotsch, A.; Wieland, A.; Schwartz, T. Ozone treatment of conditioned wastewater selects antibiotic resistance genes, opportunistic bacteria, and induce strong population shifts Sci. Total Environ. 2016, 559, 103-112 10.1016/j.scitotenv.2016.03.154
36. Lüddeke, F.; Heß, S.; Gallert, C.; Winter, J.; Güde, H.; Löffler, H. Removal of total and antibiotic resistant bacteria in advanced wastewater treatment by ozonation in combination with different filtering techniques Water Res. 2015, 69, 243-251 10.1016/j.watres.2014.11.018
37. von Gunten, U.; Hoigne, J. Bromate formation during ozonation of bromide-containing waters: Interaction of ozone and hydroxyl radical reactions Environ. Sci. Technol. 1994, 28 (7) 1234-1242 10.1021/es00056a009
38. Zimmermann, S. G.; Wittenwiler, M.; Hollender, J.; Krauss, M.; Ort, C.; Siegrist, H.; von Gunten, U. Kinetic assessment and modeling of an ozonation step for full-scale municipal wastewater treatment: Micropollutant oxidation, by-product formation and disinfection Water Res. 2011, 45 (2) 605-617 10.1016/j.watres.2010.07.080
39. Berney, M.; Weilenmann, H. U.; Egli, T. Flow-cytometric study of vital cellular functions in Escherichia coli during solar disinfection (SODIS) Microbiology 2006, 152, 1719-1729 10.1099/mic.0.28617-0
40. Bunthof, C. J.; van den Braak, S.; Breeuwer, P.; Rombouts, F. M.; Abee, T. Rapid fluorescence assessment of the viability of stressed Lactococcus lactis Appl. Environ. Microbiol. 1999, 65 (8) 3681-3689
41. Berney, M.; Vital, M.; Hülshoff, I.; Weilenmann, H.-U.; Egli, T.; Hammes, F. Rapid, cultivation-independent assessment of microbial viability in drinking water Water Res. 2008, 42 (14) 4010-4018 10.1016/j.watres.2008.07.017
42. Berney, M.; Hammes, F.; Bosshard, F.; Weilenmann, H.-U.; Egli, T. Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight Kit in combination with Flow Cytometry Appl. Environ. Microbiol. 2007, 73 (10) 3283-3290 10.1128/AEM.02750-06
43. Hammes, F.; Berney, M.; Wang, Y.; Vital, M.; Köster, O.; Egli, T. Flow-cytometric total bacterial cell counts as a descriptive microbiological parameter for drinking water treatment processes Water Res. 2008, 42 (1-2) 269-277 10.1016/j.watres.2007.07.009
44. Ramseier, M. K.; von Gunten, U.; Freihofer, P.; Hammes, F. Kinetics of membrane damage to high (HNA) and low (LNA) nucleic acid bacterial clusters in drinking water by ozone, chlorine, chlorine dioxide, monochloramine, ferrate(VI), and permanganate Water Res. 2011, 45 (3) 1490-1500 10.1016/j.watres.2010.11.016
45. CLSI. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-Third Informational Supplement, CLSI document M100-S23; Clinical and Laboratory Standards Institue: Wayne, PA, 2013.
46. Takai, K.; Horikoshi, K. Rapid detection and quantification of members of the archaeal community by quantitative PCR using fluorogenic probes Appl. Environ. Microbiol. 2000, 66 (11) 5066-5072 10.1128/AEM.66.11.5066-5072.2000
47. Poliquin, L.; Hamelin, C.; Chung, Y. S. Isolement et charactérisation de mutants sensibles ou résistant à l'ozone chez Escherichia coli B Can. J. Genet. Cytol. 1982, 24 (5) 593-600 10.1139/g82-063
48. Hunt, N. K.; Mariñas, B. J. Kinetics of Escherichia coli inactivation with ozone Water Res. 1997, 31 (6) 1355-1362 10.1016/S0043-1354(96)00394-6
49. Geeraerd, A. H.; Herremans, C. H.; Van Impe, J. F. Structural model requirements to describe microbial inactivation during a mild heat treatment Int. J. Food Microbiol. 2000, 59 (3) 185-209 10.1016/S0168-1605(00)00362-7
50. Bazin, M. J.; Prosser, J. I. Physiological Models in Microbiology; CRC Press, 1988.
51. Arana, I.; Santorum, P.; Muela, A.; Barcina, I. Chlorination and ozonation of waste-water: comparative analysis of efficacy through the effect on Escherichia coli membranes J. Appl. Microbiol. 1999, 86 (5) 883-883 10.1046/j.1365-2672.1999.00772.x
52. Lee, Y.; Imminger, S.; Czekalski, N.; von Gunten, U.; Hammes, F. Inactivation efficiency of Escherichia coli and autochthonous bacteria during ozonation of municipal wastewater effluents quantified with flow cytometry and adenosine tri-phosphate analyses Water Res. 2016, 101, 617-627 10.1016/j.watres.2016.05.089
53. Janex, M. L.; Savoye, P.; Roustan, M.; Do-Quang, Z.; Laîné, J. M.; Lazarova, V. Wastewater disinfection by ozone: influence of water quality and kinetics modeling Ozone: Sci. Eng. 2000, 22 (2) 113-121 10.1080/01919510008547215
54. Driedger, A.; Staub, E.; Pinkernell, U.; Marinas, B.; Koster, W.; Von Gunten, U. Inactivation of Bacillus subtilis spores and formation of bromate during ozonation Water Res. 2001, 35 (12) 2950-2960 10.1016/S0043-1354(00)00577-7
55. Lee, Y.; Kovalova, L.; McArdell, C. S.; von Gunten, U. Prediction of micropollutant elimination during ozonation of a hospital wastewater effluent Water Res. 2014, 64, 134-148 10.1016/j.watres.2014.06.027
56. Amann, R. I.; Ludwig, W.; Schleifer, K. H. Phylogenetic identification and in-situ detection of individual microbial-cells without cultivation Microbiol. Rev. 1995, 59 (1) 143-169
57. Oliver, J. D. The viable but nonculturable state in bacteria J. Microbiol. 2005, 43, 93-100
58. Dietrich, J. P.; Loge, F. J.; Ginn, T. R.; Başaǧaoǧlu, H. Inactivation of particle-associated microorganisms in wastewater disinfection: Modeling of ozone and chlorine reactive diffusive transport in polydispersed suspensions Water Res. 2007, 41 (10) 2189-2201 10.1016/j.watres.2007.01.038
59. Davis, I. The survival and mutability of Escherichia coli in aqueous solutions of ozone. Ph.D. Thesis, University of Pennsylvania, Philadelphia, PA, 1959.
60. Foster, P. L. Stress-induced mutagenesis in bacteria Crit. Rev. Biochem. Mol. Biol. 2007, 42 (5) 373-397 10.1080/10409230701648494
61. Substanzen zur Überprüfung des Reinigungseffekts weitergehender Abwasserbehandlungsverfahren, Fachbericht im Auftrag des Bundesamts für Umwelt BAFU; Eawag: Dübendorf, 2014;.
62. Andersson, D. I.; Hughes, D. Microbiological effects of sublethal levels of antibiotics Nat. Rev. Microbiol. 2014, 12 (7) 465-478 10.1038/nrmicro3270
63. Chow, L.; Waldron, L.; Gillings, M. Potential impacts of aquatic pollutants: Sub-clinical antibiotic concentrations induce genome changes and promote antibiotic resistance Front. Microbiol. 2015, 10.3389/fmicb.2015.00803
64. Gullberg, E.; Cao, S.; Berg, O. G.; Ilbäck, C.; Sandegren, L.; Hughes, D.; Andersson, D. I. Selection of resistant bacteria at very low antibiotic concentrations PLoS Pathog. 2011, 7 (7) e1002158 10.1371/journal.ppat.1002158
65. Jutkina, J.; Rutgersson, C.; Flach, C.-F.; Joakim Larsson, D. G. An assay for determining minimal concentrations of antibiotics that drive horizontal transfer of resistance Sci. Total Environ. 2016, 548-549, 131-138 10.1016/j.scitotenv.2016.01.044
66. Kim, S.; Yun, Z. W.; Ha, U. H.; Lee, S.; Park, H.; Kwon, E. E.; Cho, Y.; Choung, S.; Oh, J.; Medriano, C. A.; Chandran, K. Transfer of antibiotic resistance plasmids in pure and activated sludge cultures in the presence of environmentally representative micro-contaminant concentrations Sci. Total Environ. 2014, 468, 813-820 10.1016/j.scitotenv.2013.08.100
67. Schindler Wildhaber, Y.; Mestankova, H.; Scharer, M.; Schirmer, K.; Salhi, E.; von Gunten, U. Novel test procedure to evaluate the treatability of wastewater with ozone Water Res. 2015, 75, 324-335 10.1016/j.watres.2015.02.030
68. Huijbers, P. M. C.; Blaak, H.; de Jong, M. C. M.; Graat, E. A. M.; Vandenbroucke-Grauls, C. M. J. E.; de Roda Husman, A. M. Role of the Environment in the Transmission of Antimicrobial Resistance to Humans: A Review Environ. Sci. Technol. 2015, 49 (20) 11993-12004 10.1021/acs.est.5b02566