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MIAMI UNIVERSITY the Graduate School Certificate for Approving The MIAMI UNIVERSITY The Graduate School Certificate for Approving the Dissertation We hereby approve the Dissertation of Sandra J. Connelly Candidate for the Degree: Doctor of Philosophy __________________________________________ Director Dr. Craig E. Williamson __________________________________________ Reader Dr. Maria González __________________________________________ Reader Dr. David L. Mitchell __________________________________________ Graduate School Representative Dr. A. John Bailer ABSTRACT EFFECTS OF ULTRAVIOLET RADIATION (UVR) INDUCED DNA DAMAGE AND OTHER ECOLOGICAL DETERMINANTS ON CRYPTOSPORIDIUM PARVUM, GIARDIA LAMBLIA, AND DAPHNIA SPP. IN FRESHWATER ECOSYSTEMS Sandra J. Connelly Freshwater ecosystems are especially susceptible to climatic change, including anthropogenic-induced changes, as they are directly influenced by the atmosphere and terrestrial ecosystems. A major environmental factor that potentially affects every element of an ecosystem, directly or indirectly, is ultraviolet radiation (UVR). UVR has been shown to negatively affect the DNA of aquatic organisms by the same mechanism, formation of photoproducts (cyclobutane pyrimidine dimers; CPDs), as in humans. First, the induction of CPDs by solar UVR was quantified in four aquatic and terrestrial temperate ecosystems. Data show significant variation in CPD formation not only between aquatic and terrestrial ecosystems but also within a single ecosystem and between seasons. Second, there is little quantitative data on UV-induced DNA damage and the effectiveness of DNA repair mechanisms on the damage induced in freshwater invertebrates in the literature. The rate of photoproduct induction (CPDs) and DNA repair (photoenzymatic and nucleotide excision repair) in Daphnia following UVR exposures in artificial as well as two natural temperate lake systems was tested. The effect of temperature on the DNA repair rates, and ultimately the organisms’ survival, was tested under controlled laboratory conditions following artificial UVB exposure. The results of these studies suggest a significant interaction of UVR and temperature on individual survival and ultimately population dynamics in freshwater systems. Lastly, freshwater human pathogens have negative effects ranging from gastrointestinal distress in otherwise healthy individuals to death in the immunocompromised and elderly. The control of infectious pathogens in water treatment is imperative. The abiotic and biotic environmental stressors of human pathogens are not well understood. Herein, solar radiation and artificial UVB are shown to significantly decrease the infectivity of Cryptosporidium parvum in vitro. The generalist filter feeder, Daphnia pulicaria, was shown to have significant effects on the viability, excystation, and infectivity of both Cryptosporidium parvum and Giardia lamblia under laboratory- controlled conditions. Both of these studies have significant implications for the natural control and potable water pretreatment approaches to human pathogen control. EFFECTS OF ULTRAVIOLET RADIATION (UVR) INDUCED DNA DAMAGE AND OTHER ECOLOGICAL DETERMINANTS ON CRYPTOSPORIDIUM PARVUM, GIARDIA LAMBLIA, AND POTENTIAL ZOOPLANKTON GRAZERS IN FRESHWATER ECOSYSTEMS A DISSERTATION Submitted to the Faculty of Miami University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Zoology by Sandra J. Connelly Miami University Oxford, Ohio 2007 Dr. Craig E. Williamson, Miami University, Chair, Major Advisor Dr. Maria González, Miami University Dr. David L. Mitchell, MD Andersen Cancer Center, University of Texas Dr. James Oris, Miami University Dr. Michael Vanni, Miami University Dr. A. John Bailer, Miami University, Graduate School Representative © Sandra J. Connelly 2007 ii Table of Contents LIST OF TABLES IV LIST OF FIGURES IV DEDICATION VI ACKNOWLEDGEMENTS VII CHAPTER 1: INTRODUCTION AND OVERVIEW 1 CHAPTER 2: ANNUAL AND SEASONAL VARIABILITY OF UV-INDUCED DNA DAMAGE IN A TEMPERATE ECOSYSTEM ASSESSED BY DOSIMETRY 15 CHAPTER 3: EXAMINATION OF UV-INDUCED DNA DAMAGE IN DAPHNIIDS: DNA DAMAGE VS. REPAIR AT DEPTH IN TWO LAKE SYSTEMS 37 CHAPTER 4: TEMPERATURE EFFECTS ON UV-INDUCED DNA DAMAGE AND ITS REPAIR: BIOLOGICAL RESPONSES OF FOUR SPECIES OF THE FRESHWATER CLADOCERAN DAPHNIA 61 CHAPTER 5: ARTIFICIAL UV-B AND SOLAR RADIATION REDUCE IN VITRO INFECTIVITY OF THE HUMAN PATHOGEN CRYPTOSPORIDIUM PARVUM 88 CHAPTER 6: IMPACT OF ZOOPLANKTON GRAZING ON THE EXCYSTATION, VIABILITY, OR INFECTIVITY OF THE PROTOZOAN PATHOGENS CRYPTOSPORIDIUM PARVUM AND GIARDIA LAMBLIA 108 CONCLUDING REMARKS 129 iii List of Tables TABLE 2.1. AQUATIC IRRADIANCE MEASURES IN LAKES GILES AND LACAWAC (2005-2006)............................................................................................................... 24 TABLE 2.2. INCIDENT SOLAR IRRADIANCE (APRIL & JULY 2006).................................. 24 TABLE 3.1. ABIOTIC MEASUREMENTS IN LAKES GILES AND LACAWAC (APRIL – AUGUST 2006) ........................................................................................... 45 TABLE 4.1. RATE OF REPAIR ± PHOTOREPAIR RADIATION IN DAPHNIA......................... 86 TABLE 4.2. UVB RESPONSE PARAMETER COMPARISON OF DAPHNIA ............................ 87 TABLE 5.1. SOLAR EXPOSURES OF CRYPTOSPORIDIUM PARVUM (JULY & SEPTEMBER 2006) ..................................................................................... 96 TABLE 5.2. IN VITRO INFECTIVITY OF CRYPTOSPORIDIUM PARVUM FOLLOWING UVB AND SOLAR EXPOSURE.............................................................................................. 99 TABLE 6.1. CLEARANCE RATES OF CRYPTOSPORIDIUM PARVUM , GIARDIA LAMBLIA, AND SELENASTRUM BY DAPHNIA PULICARIA ................................................................. 119 TABLE 6.2. VIABILITY, EXCYSTATION, OR INFECTIVITY OF CRYPTOSPORIDIUM PARVUM AND GIARDIA LAMBLIA POST GRAZING BY DAPHNIA PULICARIA ............................ 121 iv List of Figures FIGURE 1.1: SCHEMATIC OF DISSERTATION HYPOTHESES.................................................... 5 FIGURE 2.1. TERRESTRIAL UV-INDUCED DNA DAMAGE (2005-2006) ............................. 26 FIGURE 2.2. AQUATIC UV-INDUCED DNA DAMAGE (2005-2006) .................................... 27 FIGURE 2.3. TERRESTRIAL NITRATE AND NITRITE ACTINOMETRY (APRIL & JULY 2006)... 29 FIGURE 2.4. AQUATIC NITRATE AND NITRITE ACTINOMETRY (APRIL & JULY 2006).......... 30 FIGURE 3.1. UVB LAMP EMISSION SPECTRUM ................................................................... 43 FIGURE 3.2. SEASONAL AQUATIC UV-INDUCED DNA DAMAGE (APRIL – AUGUST 2006). 54 FIGURE 4.1. UVB LAMP AND PHOTOREACTIVE RADIATION (PRR) EMISSION SPECTRA...... 67 2 FIGURE 4.2.SURVIVAL OF DAPHNIA AT TWO TEMPERATURES (20 KJ/M UVR EXPOSURE).72 FIGURE 4.3. DNA DAMAGE INDUCTION IN DAPHNIA (20 KJ/M2 UVR EXPOSURE)............. 73 FIGURE 4.4. PHOTOPROTECTION IN DAPHNIA AT 10° AND 20°C ........................................ 74 FIGURE 4.5. DNA REPAIR RATES IN DAPHNIA AT 10° AND 20°C........................................ 75 FIGURE 4.6. NON-REPAIRABLE DAMAGE IN DAPHNIA ± PHOTOREPAIR RADIATION ............ 76 FIGURE 6.1. DAPHNIA PULICARIA GUT CONTENT (CRYPTOSPORIDIUM PARVUM AND GIARDIA LAMBLIA) .................................................................................................................. 113 FIGURE 6.2. NAMARSKI CONTRAST IMAGE OF GIARDIA LAMBLIA, CRYPTOSPORIDIUM PARVUM, AND SELENASTRUM USED IN DAPHNIA PULICARIA GRAZING EXPERIMENTS .. 114 FIGURE 6.3. PERCENT CHANGE IN EXCYSTATION, VIABILITY, OR INFECTIVITY OF GIARDIA LAMBLIA OR CRYPTOSPORIDIUM PARVUM POST GRAZING BY DAPHNIA PULICARIA ...... 122 v Dedication To all those who have shared in this journey – we made it! This final compilation of many years of work, which was full of both great achievements and heart-wrenching failures, was only possible through the support, compassion, and unending love of my family, my boyfriend, and the amazing network of friends that I have amassed over the years. My mother and father have taught me that only through hard work and persistence will we ever prove to ourselves how great we can be. My siblings have taught me that no matter the problems that life throws at you, it is nothing that a little ice cream can’t fix! My boyfriend has taught me that anything can be overcome if you are passionate. My friends have taught me that life is not life without the love of friends and that when all else fails, friends will never fail you. This dissertation is dedicated to these people, and so many more. Seemingly insurmountable mountains were no more than pebbles in the road because of you – thank you. vi Acknowledgements The work herein would never have been possible without the guidance, support, and undying commitment of my major advisor, Dr. Craig Williamson, my DNA damage mentor, Dr. David Mitchell, and my pathogen mentor, Dr. Kristen Jellison. They have taught me so much and helped me grow not only as a scientist and teacher, but as a person. Thank you. Thanks to my doctoral committee and the Department of Zoology at Miami for being so amenable during my transfer between Universities. A special thanks to the members of the Williamson Ecology of UV Lab, past and present, especially Dr. Robert Moeller, Erin Overholt, and Dr. Gaby Dee for both the positive and negative critiques through the years! Without them both, I would have never made it this far! Thanks to the students and technicians that have been a driving force in my research, both in the lab and the field, through the years. Thanks to the undergraduates
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