Inactivation efficiency of Escherichia coli and autochthonous bacteria during ozonation of municipal wastewater effluents quantified with flow cytometry and adenosine tri-phosphate analyses

Water Research

Volumn 101, Issue , 2016, Pages 617-627

  Lee, Yunho ^a,b   Imminger, Stefanie ^a   Czekalski, Nadine ^a   von Gunten, Urs ^a,c,d   Hammes, Frederik ^a  

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

^b Gwangju Institute of Science and Technology (GIST)   (South Korea)

^c ETH ZURICH   (Switzerland)

^d EPFL   (Switzerland)

Author keywords

Adenosine tri phosphate (ATP); Disinfection; Escherichia coli; Flow cytometry (FCM); Municipal wastewater effluent; Ozonation

Indexed keywords

ADENOSINETRIPHOSPHATE; EFFLUENTS; ESCHERICHIA COLI; FLOW CYTOMETRY; OZONE; OZONE WATER TREATMENT; WASTEWATER TREATMENT;

ADENOSINE TRI PHOSPHATES; ADENOSINE TRI-PHOSPHATE; AUTOCHTHONOUS BACTERIA; CELL COUNT; FLOW CYTOMETRY; INTACT CELLS; MUNICIPAL WASTEWATER EFFLUENT; MUNICIPAL WASTEWATERS; OZONE DOSE; WASTEWATER EFFLUENTS;

OZONIZATION;

ADENOSINE TRIPHOSPHATE; OZONE; ADENOSINE; PHOSPHATE;

BACTERIUM; DISINFECTION; EFFLUENT; ENZYME; FLOW CYTOMETRY; KINETICS; LABORATORY METHOD; MUNICIPAL SOLID WASTE; OZONE; WASTEWATER;

ARTICLE; BACTERIAL CELL; BACTERIUM CULTURE; ESCHERICHIA COLI; FLOW CYTOMETRY; LIMIT OF DETECTION; MUNICIPAL WASTEWATER EFFLUENT; NONHUMAN; OZONATION; PRIORITY JOURNAL; WASTE WATER; WATER QUALITY; BACTERIUM; SEWAGE;

ESCHERICHIA COLI;

ADENOSINE; ADENOSINE TRIPHOSPHATE; BACTERIA; ESCHERICHIA COLI; FLOW CYTOMETRY; OZONE; PHOSPHATES; WASTE DISPOSAL, FLUID; WASTE WATER;

EID: 84974816067     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2016.05.089     Document Type: Article

References (42)

1. Alexander J., Knopp G., Dötsch 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.
2. 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.
3. 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, 73:3283-3290.
4. 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, 42:4010-4018.
5. Blatchley E.R., Weng S., Afifi M.Z., Chiu H.H., Reichlin D.B., Jousset S., Erhardt R.S. Ozone and UV254 radiation for municipal wastewater disinfection. Water Environ. Res. 2012, 84:2017-2027.
6. 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, 14:1754-1771.
7. Driedger A., Staub E., Pinkernell U., Mariñas B., Köster W., von Gunten U. Inactivation of Bacillus subtilis spores and formation of bromate during ozonation. Water Res. 2001, 35:2950-2960.
8. Finch G.R., Fairbairn N. Comparative inactivation of poliovirus type 3 and MS2 coliphage in demand-free phosphate buffer by using ozone. Appl. Environ. Microbiol. 1991, 57:3121-3126.
9. Finch G.R., Black E.K., Labatiuk C.W., Cyürék L., Belosevic M. Comparison of Giardia lamblia and Giardia muris cyst inactivation by ozone. Appl. Environ. Microbiol. 1993, 59:3674-3680.
10. Gamage S., Gerrity D., Pisarenko A.N., Wert E.C., Snyder S.A. Evaluation of process control alternatives for the inactivation of Escherichia coli, MS2 bacteriophage, and Bacillus subtilis spores during wastewater ozonation. Ozone Sci. Eng. 2013, 35:501-513.
11. Greenstock C.L., Shierman E. Radiosensitivity and hydroxyl radical reactivity of phosphate esters as measured by radiation-induced dephosphorylation. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 1975, 28:1-11.
12. 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, 42:269-277.
13. Hammes F., Goldschmidt F., Vital M., Wang Y., Egli T. Measurement and interpretation of microbial adenosine triphosphate (ATP) in aquatic environments. Water Res. 2010, 44:3915-3923.
14. Hammes F., Berney M., Egli T. Cultivation-independent assessment of bacterial viability. Adv. Biochem. Eng. Biotechnol. 2011, 124:123-150.
15. Hoefel D., Monis P.T., Grooby W.L., Andrews S., Saint C.P. Culture-independent techniques for rapid detection of bacteria associated with loss of chloramine residual in a drinking water system. Appl. Environ. Microbiol. 2005, 71:6479-6488.
16. Huber M.M., Göbel A., Joss A., Hermann N., Löffler D., Mcardell C.S., Ried A., Siegrist H., Ternes T.A., von Gunten U. Oxidation of pharmaceuticals during ozonation of municipal wastewater effluents: a pilot study. Environ. Sci. Technol. 2005, 39:4290-4299.
17. Hunt N.K., Mariñas B.J. Inactivation of Escherichia coli with ozone: chemical and inactivation kinetics. Water Res. 1999, 33:2633-2641.
18. Jacangelo J.G., Trussell R.R. International report: water and wastewater disinfection-trends, issues, and practices. Water Sci. Technol. Water Supply 2002, 2:147-157.
19. Lee Y., von Gunten U. Quantitative structure-activity relationships (QSARs) for the transformation of organic micropollutants during oxidative water treatment. Water Res. 2012, 46:6177-6195.
20. 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, 47:5872-5881.
21. Lee Y., von Gunten U. Advances in predicting organic contaminant abatement during ozonation of municipal wastewater effluent: reaction kinetics, transformation products, and changes of biological effects. Environ. Sci. Water Res. Technol. 2016, 2:421-442.
22. Loeb B.L., Thompson C.M., Drago J.D., Takahara H., Baig S. Worldwide ozone capacity for treatment of drinking water and wastewater: a review. Ozone Sci. Eng. 2012, 34:64-77.
23. Lisle J.T., Pyle B.H., McFeters G.A. The use of multiple indices of physiological activity to access viability in chlorine disinfected Escherichia coli O157:H7. Lett. Appl. Microbiol. 1999, 29:42-47.
24. Lüddeke F., He 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.
25. Magdeburg A., Stalter D., Schlüsener M., Ternes T., Oehlmann J. Evaluating the efficiency of advanced wastewater treatment: target analysis of organic contaminants and (geno-)toxicity assessment tell a different story. Water Res. 2014, 50:35-47.
26. Nocker A., Camper A.K. Novel approaches toward preferential detection of viable cells using nucleic acid amplification techniques. FEMS Microbiol. Lett. 2009, 291:137-142.
27. Oneby M.A., Bromley C.O., Borchardt J.H., Harrison D.S. Ozone treatment of secondary effluent at U.S. municipal wastewater treatment plants. Ozone Sci. Eng. 2010, 32:43-55.
28. Paraskeva P., Graham N.J.D. Ozonation of municipal wastewater effluents. Water Environ. Res. 2002, 74:569-581.
29. Phe M.-H., Dossot M., Guilloteau H., Block J.-C. Nucleic acid fluorochromes and flow cytometry prove useful in assessing the effect of chlorination on drinking water bacteria. Water Res. 2005, 39:3618-3628.
30. Prest E.I., Hammes F., Kötzsch S., van Loosdrecht M.C.M., Vrouwenwelder J.S. Monitoring microbiological changes in drinking water systems using a fast and reproducible flow cytometric method. Water Res. 2013, 47:7131-7142.
31. Pruden A. Balancing water sustainability and public health goals in the face of growing concerns about antibiotic resistance. Environ. Sci. Technol. 2014, 48:5-14.
32. 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, 45:1490-1500.
33. Rennecker J.L., Mariñas B.J., Owens J.H., Rice E.W. Inactivation of Cryptosporidium parvum oocysts with ozone. Water Res. 1999, 33:2481-2488.
34. Theruvathu J.A., Flyunt R., Aravindakumar C.T., von Sonntag C. Rate constants of ozone reactions with DNA, its constituents and related compounds. J. Chem. Soc. Perkin Trans. 2001, 2:269-274.
35. van Nevel S., Koetzsch S., Weilenmann H.-U., Boon N., Hammes F. Routine bacterial analysis with automated flow cytometry. J. Microbiol. Methods 2013, 94:73-76.
36. Varela Villarreal J., Jungfer C., Obst U., Schwartz T. DNase I and Proteinase K eliminate DNA from injured or dead bacteria but not from living bacteria in microbial reference systems and natural drinking water biofilms for subsequent molecular biology analyses. J. Microbiol. Method 2013, 94:161-169.
37. von Sonntag C., von Gunten U. Chemistry of Ozone in Water and Wastewater Treatment: From Basic Principles to Applications 2012, IWA Publishing, London.
38. Wang Y., Hammes F., De Roy K., Verstraete W., Boon N. Past, present, and future applications of flow cytometry in aquatic microbiology. Trends Biotechnol. 2010, 28:416-424.
39. Xu P., Janex M.-L., Savoye P., Cockx A., Lazarova V. Wastewater disinfection by ozone: main parameters for process design. Water Res. 2002, 36:1043-1055.
40. 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, 45:605-617.
41. Zhuang Y., Ren H., Geng J., Zhang Y., Zhang Y., Ding L., Xu K. Inactivation of antibiotic resistance genes in municipal wastewater by chlorination, ultraviolet, and ozonation disinfection. Environ. Sci. Pollut. Res. 2015, 22:7037-7044.
42. Zipper H., Brunner H., Bernhagen J., Vitzthum F. Investigations on DNA intercalation and surface binding by SYBR Green I, its structure determination and methodological implications. Nucleic Acids Res. 2004, 32:e103.