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Upper and Lower Case Letters to Be Used Isolation, characterization and genome sequencing of a soil-borne Citrobacter freundii strain capable of detoxifying trichothecene mycotoxins by Rafiqul Islam A Thesis Presented to The University of Guelph In Partial Fulfilment of Requirements for the Degree of Doctor of Philosophy in Plant Agriculture Guelph, Ontario, Canada © Rafiqul Islam, April, 2012 ABSTRACT ISOLATION, CHARACTERIZATION AND GENOME SEQUENCING OF A SOIL- BORNE CITROBACTER FREUNDII STRAIN CAPABLE OF DETOXIFIYING TRICHOTHECENE MYCOTOXINS Rafiqul Islam Advisors: University of Guelph, 2012 Dr. K. Peter Pauls Dr. Ting Zhou Cereals are frequently contaminated with tricthothecene mycotoxins, like deoxynivalenol (DON, vomitoxin), which are toxic to humans, animals and plants. The goals of the research were to discover and characterize microbes capable of detoxifying DON under aerobic conditions and moderate temperatures. To identify microbes capable of detoxifying DON, five soil samples collected from Southern Ontario crop fields were tested for the ability to convert DON to a de-epoxidized derivative. One soil sample showed DON de-epoxidation activity under aerobic conditions at 22-24°C. To isolate the microbes responsible for DON detoxification (de-epoxidation) activity, the mixed culture was grown with antibiotics at 50ºC for 1.5 h and high concentrations of DON. The treatments resulted in the isolation of a pure DON de-epoxidating bacterial strain, ADS47, and phenotypic and molecular analyses identified the bacterium as Citrobacter freundii. The bacterium was also able to de-epoxidize and/or de-acetylate 10 other food-contaminating trichothecene mycotoxins. A fosmid genomic DNA library of strain ADS47 was prepared in E. coli and screened for DON detoxification activity. However, no library clone was found with DON detoxification activity. The whole genome of ADS47 was also sequenced, and from comparative genome analyses, 10 genes (characterized as reductases, oxidoreductases and deacetylase) were identified as potential candidates for DON/trichothecene detoxifying enzymes. Bioinformatic analyses showed that the major animal pathogenic locus of enterocyte effacement (LEE) operon genes absent from the ADS47 genome. Strain ADS47 has the potential to be used for feed detoxification and the development of mycotoxin resistance cereal cultivars. DEDICATIONS The Ph.D. thesis is dedicated to the departed souls of my mother MOZIBUN NESSA and father-in-law DR. M.A. AHAD MIAH iii ACKNOWLEDGEMENTS Foremost, I am deeply indebted to my advisors Prof. K. Peter Pauls and Dr. Ting Zhou for the continuous support of my Ph.D. study; for their endurance, inspiration, enthusiasm and mentoring. Their continued guidance has helped me in all aspects of my research and in writing of this dissertation. I sincerely express my gratitude to them for their co-operation from the beginning to conclusion of the thesis and many other areas. This will guide me in my future professional career. My thesis committee guided me through all these years. I would like to express my gratitude to Prof. Paul Goodwin for his insightful comments and advice on my thesis research. Special thanks to Dr. Chris Young for teaching me chemistry, chemical structures and interpreting liquid chromatography ultraviolet mass spectra data. I am sincerely grateful to Dion Lepp for helping in analyzing the bacterial genome and sharing his knowledge and valuable suggestions on writing the genomic chapter. I would like to express my appreciation to staff members of Dr. Ting Zhou and Prof. K. Peter Pauls who supported me in many aspects during my PhD study. I am thankful to Jianwei He, Xiu-Zhen Li, Honghui Zhu for collections and preparation of soil samples and LC-UV-MS analyses of numerous samples. Special thanks to Dr. David Morris Johnston Monje for sharing his knowledge, discussions and camaraderie at coffee breaks. I wish to acknowledge the Natural Sciences and Engineering Research Council of Canada (NSERC) for awarding me a prestigious scholarship for my Ph.D. program and Dean’s Tri-Council Scholarship (University of Guelph), which made my life easier during this study. I also would like to convey my thanks to Agriculture and Agri-Food Canada/Binational iv Agricultural Research and Development Fund (AAFC/BARD) project for providing me financial support. Mike Bryan, a very supportive person, helped provide solutions to my software issues that improved my exposure and caliber at conference awards competitions. Several student competition awards honored and inspired me to work hard and lead to the successful completion of my thesis research. I would like to convey my appreciation to the judges of different student award committees who recognized my work. They are: Society for Industrial Microbiology and Biotechnology conference 2010 (USA); Food Safety Research Forum- Ontario Ministry of Agriculture and Rural Affairs annual meeting 2010 (Canada); International Mycological Conference 2009 (UK); and Southwestern Ontario Regional Association of Canadian Phytopathological Society annual meeting 2009-2011 (Canada). I would like to express my very special thanks to Prof. Golam Hafeez Kennedy, my brother-in-law, who is like my elder brother. In many aspects I am indebt to him for his cooperations which aided me to achieve my current status. Lastly, and most importantly, I wish to give my special thanks to my wife Mimi and lovely daughter Racy, whose endless love, sacrifice, support and encouragement enabled me to cross the tough long road and made possible to achieve my goal and aspirations. Racy, once you told me that one of your desires for me is to finish my Ph.D., which is done now. I know you want to be a scientist, which is a great ambition. I wish you all the best in your future aims Racy. v TABLE OF CONTENTS DEDICATIONS…………………………………………………………………………...…iii ACKNOWLEDGEMENTS…………………………………………………………………iv TABLE OF CONTENTS……………………………………………………………………vi LIST OF TABLES…………………………………………………………………………...ix LIST OF FIGURES………………………………………………………………………......x LIST OF ABBREVIATIONS……………………………………………………………...xiii 1.0. GENERAL INTRODUCTION AND LITERATURE REVIEW …………………….1 1.1. Background………………………………………………………………………………..1 1.2. Plant pathogenesis and trichothecene production…………………………………………3 1.3. Biosynthesis of food contaminating TC…………..……………………………………….6 1.4. Occurrence of TC mycotoxins in food and feed ………………………………………...11 1.5. Significance of deoxynivalenol and trichothecenes……………………………………...16 1.6. Toxic effects of deoxynivalenol and trichothecenes……………………………………..19 1.7. Cellular and molecular mechanisms of DON toxicity in animals and plants…….……...22 1.8. Strategies to control Fusarium head blight and trichothecenes...………………………..26 1.9. Isolation of DON/TC de-epoxidating micro-organisms and genes………………….…...28 1.10. The bacterial species Citrobacter freundii……………………………………………...30 1.11. Hypotheses and objectives………………………………………………………..…….31 vi 2.0. AEROBIC AND ANAEROBIC DE-EPOXIDATION OF MYCOTOXIN DEOXYNIVALENOL BY BACTERIA ORIGINATING FROM AGRICULTURAL SOIL...................................................................................................................................33 2.1. Abstract ………………………………………………………………………………….33 2.2. Introduction ……………………………………………………………………………...34 2.3. Materials and methods…………………………………………………………………...37 2.4. Results …………………………………………………………………………………...45 2.5. Discussion………………………………………………………………………………..62 2.6. Acknowledgements………………………………………………………………………64 3.0. ISOALTION AND CHARACTERIZATION OF A NOVEL SOIL BACTERIUM CAPABLE OF DETOXIFYING ELEVEN TRICHOTHECENE MYCOTOXINS..65 3.1. Abstract ………………………………………………………………………………….65 3.2. Introduction ……………………………………………………………………………..66 3.3. Materials and methods…………………………………………………………………...68 3.4. Results …………………………………………………………………………………...75 3.5. Discussion………………………………………………………………………………..96 3.6. Acknowledgements……………………………………………………………………..100 4.0. CONSTRUCTION AND FUNCTIONAL SCREENING OF GENOMIC DNA LIBRARY FOR ISOLATION OF DON DE-EPOXYDIZING GENE(S) FROM BACTERIAL STRAIN ADS47……………………......................................................102 4.1. Abstract ………………………………………………………………………………...102 4.2. Introduction …………………………………………………………………………….103 4.3. Materials and methods………………………………………………………………….104 vii 4.4. Results ………………………………………………………………………………….112 4.5. Discussion………………………………………………………………………………118 4.6. Acknowledgements……………………………………………………………………..121 5.0. GENOME SEQUENCING, CHARACTERIZATION AND COMPARATIVE ANALYSIS OF A TRICHOTHECENE MYCOTOXIN DETOXIFYING CITROBACTER FREUNDII STRAIN ADS47…………………………………….....122 5.1. Abstract ………………………………………………………………………………...122 5.2. Introduction …………………………………………………………………………….123 5.3. Materials and methods………………………………………………………………….125 5.4. Results ………………………………………………………………………………….129 5.5. Discussion………………………………………………………………………………162 5.6. Acknowledgements……………………………………………………………………..168 6.0. CONCLUSION………………………………………………………………………...171 6.1. Summary ……………………………………………………………………………….171 6.2. Research contributions …………………………………………………………………174 6.3. Future work……………………………………………………………………………..175 7.0. REFERENCES………………………………………………………………………...176 viii LIST OF TABLES Table 1-1. Fusaria produced type-A and type-B trichothecene mycotoxins…………………..9 Table 1-2. Worldwide occurrence of deoxynivalenol (DON) in animal feeds…………….....12 Table 1-3. Occurrence of DON in Canadian grains, grains foods and beers…………………13 Table 1-4. Legislative maximum tolerated levels of trichothecene mycotoxins in Canada….14 Table 1-5. In vitro and in vivo synergistic effects of
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