Inactivation and repair of escherichia coli following UV disinfection influencing factors and photolyase activity

INACTIVATION AND REPAIR OF ESCHERICHIA COLI FOLLOWING UV DISINFECTION: INFLUENCING FACTORS AND PHOTOLYASE ACTIVITY QUEK PUAY HOON ELAINE NATIONAL UNIVERSITY OF SINGAPORE 2008 INACTIVATION AND REPAIR OF ESCHERICHIA COLI FOLLOWING UV DISINFECTION: INFLUENCING FACTORS AND PHOTOLYASE ACTIVITY QUEK PUAY HOON ELAINE (B. Eng., NUS) A THESIS SUBMITTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY DEPARTMENT OF CIVIL ENGINEERING NATIONAL UNIVERSITY OF SINGAPORE 2008 ACKNOWLEDGEMENTS First and foremost, I would like to express my gratitude to my supervisor, Associate Professor Hu Jiangyong. Her patient guidance and insightful comments throughout the duration of the course have greatly contributed to the research conducted and the writing of the thesis. I wish also to extend my thanks to the laboratory manager, Mr Michael Tan, and the laboratory officers, especially Mdm Tan Xiaolan and Mr Chandra. Their expertise in microbiological techniques and laboratory procedures allowed the experiments to be conducted smoothly, while their timely advice has helped me tackle problems during the experiments. In addition, many thanks go out to my fellow postgraduate students and research staff in the laboratory, especially those in the “UV group”, who have made the hectic times in the laboratory very enjoyable. The camaraderie among the postgraduate students has created a highly conducive environment for working. Last but not least, my utmost gratitude goes to my parents, sister and my fiancé, for their constant encouragement, support and understanding throughout the last years, without which this thesis would not have been possible. i TABLE OF CONTENTS Page ACKNOWLEDGEMENTS i TABLE OF CONTENTS ii SUMMARY vii NOMENCLATURE x LIST OF TABLES xii LIST OF FIGURES xiii CHAPTER INTRODUCTION 1.1 Disinfection in Drinking Water Treatment 1.2 The Need for Alternative Disinfectants 1.3 Rise of UV Disinfection 1.4 DNA Repair – A Potential Drawback of UV Disinfection 1.5 Problem Statements 1.5.1 DNA repair following LP & MP UV disinfection 1.5.2 Factors affecting photoreactivation 1.5.3 Photoreactivation suppression by MP UV disinfection 1.6 Research Scope and Objectives 10 1.7 Organization of Thesis 13 CHAPTER CURRENT STATE OF THE ART IN UV DISINFECTION 16 2.1 Historical Development of UV Disinfection 16 2.2 Definition of UV Disinfection 18 ii Table of Contents 2.3 UV Radiation Sources & UV Disinfection Systems 20 2.3.1 UV radiation sources 20 2.3.2 UV disinfection systems 24 2.4 UV Disinfection Mechanism 30 2.5 Factors affecting UV Disinfection 33 2.5.1 UV absorbance 33 2.5.2 Particle content 34 2.5.3 Intrinsic resistance of microorganisms 37 2.6 Advantages and Disadvantages of UV Disinfection 39 2.7 Applications of UV Disinfection 40 2.8 A Potential Problem in UV Disinfection: DNA Repair 43 2.9 Photoreactivation and the role of photolyases 44 2.9.1 Definition of photolyase and properties of photolyases 44 2.9.2 Photoreactivation mechanism 47 2.9.3 Photoreactivation of microorganisms after UV disinfection 50 2.9.4 Factors affecting photoreactivation 53 2.9.5 Dark repair 58 UV Disinfection and DNA Repair of Escherichia coli 59 2.10.1 UV disinfection of E. coli 59 2.10.2 DNA repair of E. coli 61 CHAPTER MATERIALS AND METHODS 66 3.1 Overview 66 3.2 Cellular-level Study 66 2.10 iii Table of Contents 3.2.1 Bacteria strains 66 3.2.2 UV disinfection 68 3.2.3 Photoreactivation and dark repair 70 3.2.4 Bacteria enumeration 74 3.2.5 Data analysis using percentage log repair 74 Sub-cellular Level Study 76 3.3.1 Preparation of photolyase 77 3.3.2 UV irradiation of photolyase in vitro 79 3.3.3 Spectrophotometric assay for determination of photolyase activity in vitro 80 3.3.4 Molecular detection of DNA repair 86 CHAPTER INDICATORS FOR PHOTOREACTIVATION AND DARK REPAIR STUDIES FOLLOWING UV DISINFECTION 88 4.1 Background 88 4.2 UV Inactivation of E. coli 90 4.3 Photoreactivation of E. coli following UV Disinfection 94 4.4 Dark Repair of E. coli following UV Disinfection 100 4.5 Comparison of Repair of Selected Indicators and E. coli O157:H7 104 4.6 Photoreactivation of Selected Indicator at High UV Doses 106 4.7 Photoreactivation of E. coli ATCC 15597 using ESS assay 109 4.8 Summary 114 3.3 iv Table of Contents CHAPTER PHOTOREACTIVATION OF ESCHERICHIA COLI FOLLOWING UV DISINFECTION: EFFECTS OF INCUBATION TEMPERATURE & LIGHT INTENSITY 115 5.1 Background 115 5.2 Effect of Fluorescent Light Intensity on Photoreactivation 117 5.3 Effect of Sunlight Intensity on Photoreactivation 120 5.4 Fluorescent Light vs Sunlight for Photoreactivation 126 5.5 Effect of Temperature on Photoreactivation 129 5.6 Photoreactivation of E. coli ATCC 11229 vs E. coli ATCC 15597 134 5.7 Summary 135 CHAPTER IN VITRO EFFECTS OF UV RADIATION ON ESCHERICHIA COLI DNA PHOTOLYASE: IMPLICATIONS ON PHOTOREACTIVATION FOLLOWING UV DISINFECTION 136 6.1 Background 136 6.2 Characteristics of Purified Photolyase 138 6.3 Effect of UV Radiation on Photolyase Activity 140 6.4 Effect of UV Radiation on Photolyase Activity in the Presence of Dithiothreitol 145 6.5 Effect of Wavelengths in MP UV Radiation on Photolyase Activity 148 6.5.1 Varying intensities of filtered radiation 151 6.5.2 Varying wavelengths at fixed intensity 154 6.6 Comparison of Photolyase Activity following Exposure to LP, Filtered and Full-spectrum MP UV Radiation 157 6.7 Summary 158 v Table of Contents CHAPTER CONCLUSIONS & RECOMMENDATIONS FOR FUTURE STUDY 160 7.1 Conclusions 160 7.2 Limitations and Recommendations for Future Study 164 REFERENCES 167 LIST OF PUBLICATIONS 183 vi SUMMARY DNA repair following UV disinfection is a potential problem in the use of UV disinfection technology for drinking water treatment. In this thesis, photoreactivation and dark repair of Escherichia coli following UV disinfection were examined at the cellular and sub-cellular levels. At the cellular level, the repair abilities of various E. coli strains with different characteristics were studied and compared to that of pathogenic E. coli O157:H7. Up to 80% log repair was achieved with photoreactivation, while dark repair resulted in a maximum of 25% log repair. Based on repair rates, E. coli ATCC 15597 and ATCC 11229 were selected as the photoreactivation and dark repair indicators, respectively, following both low-pressure (LP) and medium-pressure (MP) UV disinfection. These indicators were also assessed for their photoreactivation levels under varying conditions of temperature and light intensity. E. coli ATCC 15597 was shown to achieve higher photoreactivation levels than E. coli ATCC 11229 under all conditions tested. Photoreactivation with fluorescent lights was also higher than that with high intensity sunlight due to the germicidal effects of sunlight, suggesting that photoreactivation levels in the natural environment could be overestimated when photoreactivation studies were conducted with fluorescent lights. Temperature affected photoreactivation to a lesser extent than light intensity, although it was observed that higher photoreactivation levels were achieved at incubation temperatures close to the optimum growth temperatures of E. coli. The results were similar for both LP and MP UV disinfection. vii Abstract On the sub-cellular level, repair of DNA was analyzed using the endonuclease sensitive site (ESS) assay. The results showed that the UV radiation-induced dimers were removed continuously with time after UV irradiation. This confirms that the increase in E. coli concentrations observed in the cellular level study was a result of the repair of dimers in DNA. Light repair was also confirmed to be more efficient than dark repair in the removal of dimers. Other than the molecular level study, the photoreactivating enzyme, photolyase, was extracted and purified from E. coli, and assessed for its dimer repair ability in vitro following exposure to LP and MP UV disinfection. The dimer repair rates of photolyase were unaffected by LP UV disinfection up to a UV dose of 10 mJ/cm2, after which the rates started to decrease with increasing UV doses up to 40 mJ/cm2. On the other hand, photolyase exposed to MP UV radiation showed an immediate decrease in dimer repair rates which leveled off so that the dimer repair rates were similar to that of LP-irradiated photolyase at 40 mJ/cm2. The results suggest that there is an adverse effect of UV radiation on dimer repair by photolyase, which most likely led to the decreased photoreactivation levels at high UV doses and with MP UV radiation. 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(2003) Inactivation and potential repair of Cryptosporidium parvum following low- and medium-pressure ultraviolet irradiation, Water Research, 37:3517-3523 182 LIST OF PUBLICATIONS The contents of this thesis have been published as articles in the following journals and have been presented at the following conferences. 1. Hu, J.Y. and P.H. Quek (2008) Effects UV Radiation on Photolyase and Implications with regards to Photoreactivation following Low- and Mediumpressure UV disinfection, Applied and Environmental Microbiology, 74(1), 327328. 2. Quek, P.H. and J.Y. Hu. (2008) Influence of Photoreactivating Light Intensity and Incubation Temperature on Photoreactivation of Escherichia coli following LP and MP UV Disinfection, Journal of Applied Microbiology, 105, 124-133 3. Quek, P.H. and J.Y. Hu. (2008) Indicators for Photoreactivation and Dark Repair Studies following Ultraviolet Disinfection, Journal of Industrial Microbiology and Biotechnology, 35(6), 533-541. 4. Quek, P.H. and J.Y. Hu. (2008) Effects of wavelengths of medium-pressure ultraviolet radiation on photolyase and subsequent photoreactivation, Journal of Applied Microbiology (submitted). 5. Quek, P.H. and J.Y. Hu. (2006) Effect of light intensity and temperature on photoreactivation of E. coli following LP and MP UV disinfection, 13th KKNN Symposium, 21 – 24 June 2006, Kyoto, Japan 6. Quek, P.H. and J.Y. Hu. (2007) Indicators for Photoreactivation and Dark Repair Studies following Ultraviolet Disinfection, 4th International Water Association Leading Edge Technologies on Water and Wastewater Technologies, – June 2007, Singapore 183 [...]... for 5-log inactivation of various Escherichia coli strains 93 Table 4-2 Photoreactivation data for Escherichia coli strains ATCC 15597 and ATCC 700891 following LP and MP UV disinfection 99 Table 4-3 Dark repair data for Escherichia coli strains ATCC 15597 and ATCC 700891 following LP and MP UV disinfection 103 Table 5-1 Percentage log recovery of E coli ATCC 11229 and ATCC 15597 following 4 h of fluorescent... h of fluorescent light and sunlight exposure with LP and MP UV disinfection 126 Table 5-2 Comparison of repair rates of E coli ATCC 11229 and ATCC 15597 following LP UV disinfection and incubation under varying light and temperature conditions 130 Table 6-1 Rate of dimer repair of LP- and MP -UV irradiated photolyase with and without DTT addition 147 xii List of Figures LIST OF FIGURES Page Figure 1-1... cultures of E coli NCIMB 10083 after exposure to fluorescent light following MP UV disinfection 97 Figure 4-4 Photoreactivation rates of various E coli strains following LP and MP UV disinfection 99 Figure 4-5 Percentage log repair of various E coli strains after incubation in the dark following (A) LP and (B) MP UV disinfection 101 Figure 4-6 Comparison of the final log concentrations of E coli O157:H7 and. .. presence of photolyase in various steps of purification 138 Figure 6-2 UV- VIS absorption spectrum of purified photolyase (diluted tenfold with assay buffer) 139 Figure 6-3 Repair rates of photolyase exposed to varying doses of LP and MP UV radiation 141 Figure 6-4 Repair rates of photolyase exposed to varying doses of LP and MP UV radiation, and chemically reduced by the addition of 5 mM DTT 146 xv List of. .. temperature and UV doses on photoreactivation of E coli after LP and MP UV disinfection • To compare photoreactivation of E coli under fluorescent light and sunlight after UV disinfection • To evaluate the effects of LP and MP UV disinfection on E coli photolyase in vitro and the subsequent impact on photoreactivation, in order to elucidate the possible mechanism for photoreactivation suppression by MP UV disinfection. .. Introduction photolyase, and therefore, photoreactivation In the entire study, the effects of various operating conditions such as UV lamp types (LP or MP UV lamp) and UV doses on repair of E coli will also be evaluated and discussed DNA Repair of Escherichia coli after UV Disinfection Comparison and confirmation of results from both studies Cellular level study Indicators for photoreactivation and dark repair. .. Sub-cellular level study Effects of environmental and operational conditions on photoreactivation Temperature and Light Intensity Dimer repair with ESS assay UV doses and Lamp types Photolyase activity in vitro Effect of UV radiation on photolyase Effects of different UV wavelengths on photolyase Overall Target of Study: To advance the understanding of DNA repair after UV disinfection, in particular photoreactivation,... Increase in A260 of photolyase- substrate mixture with time of exposure to photoreactivating light at 365 nm 84 Figure 4-1 UV inactivation of various E coli strains by (A) LP and (B) MP UV disinfection 91 Figure 4-2 Percentage log repair of various E coli strains after exposure to fluorescent light following (A) LP and (B) MP UV disinfection 95 Figure 4-3 Photoreactivation of log phase (4 h) and stationary... photoreactivation and how the interaction among the various wavelengths present in MP UV radiation can affect photoreactivation 1.6 Research Scope and Objectives In this thesis, the inactivation and repair of the model bacteria, Escherichia coli, following LP and MP UV disinfection is examined, with the main focus on the photoreactivation of E coli In particular, the repair potential of the model bacteria following. .. resulting in the reactivation of the bacteria after the water leaves the treatment plant and re-contamination of the treated water As a result of the DNA repair processes, the overall efficiency of UV disinfection is reduced and this is particularly significant when visible light exposure following UV disinfection is involved Reactivation of bacteria following UV disinfection is of great consequence, so . Photoreactivation of E. coli following UV Disinfection 94 4.4 Dark Repair of E. coli following UV Disinfection 100 4.5 Comparison of Repair of Selected Indicators and E. coli O157:H7 104 . INACTIVATION AND REPAIR OF ESCHERICHIA COLI FOLLOWING UV DISINFECTION: INFLUENCING FACTORS AND PHOTOLYASE ACTIVITY QUEK PUAY HOON ELAINE NATIONAL UNIVERSITY OF SINGAPORE. Applications of UV Disinfection 40 2.8 A Potential Problem in UV Disinfection: DNA Repair 43 2.9 Photoreactivation and the role of photolyases 44 2.9.1 Definition of photolyase and properties of photolyases