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A Systems-Level Investigation of the Metabolism of Dehalococcoides Mccartyi and the Associated Microbial Community

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A Systems-Level Investigation of the Metabolism of Dehalococcoides Mccartyi and the Associated Microbial Community A Systems-Level Investigation of the Metabolism of Dehalococcoides mccartyi and the Associated Microbial Community by Mohammad Ahsanul Islam A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Chemical Engineering and Applied Chemistry University of Toronto © Copyright by Mohammad Ahsanul Islam 2014 A Systems-Level Investigation of the Metabolism of Dehalococcoides mccartyi and the Associated Microbial Community Mohammad Ahsanul Islam Doctor of Philosophy Department of Chemical Engineering and Applied Chemistry University of Toronto 2014 Abstract Dehalococcoides mccartyi are a group of strictly anaerobic bacteria important for the detoxification of man-made chloro-organic solvents, most of which are ubiquitous, persistent, and often carcinogenic ground water pollutants. These bacteria exclusively conserve energy for growth from a pollutant detoxification reaction through a novel metabolic process termed organohalide respiration. However, this energy harnessing process is not well elucidated at the level of D. mccartyi metabolism. Also, the underlying reasons behind their robust and rapid growth in mixed consortia as compared to their slow and inefficient growth in pure isolates are unknown. To obtain better insight on D. mccartyi physiology and metabolism, a detailed pan- genome-scale constraint-based mathematical model of metabolism was developed. The model highlighted the energy-starved nature of these bacteria, which probably is linked to their slow growth in isolates. The model also provided a useful framework for subsequent analysis and visualization of high-throughput transcriptomic data of D. mccartyi. Apart from confirming expression of the majority genes of these bacteria, this analysis helped review the annotations of ii metabolic genes. Revised annotations of two such metabolic genes — NADP+-isocitrate dehydrogenase and phosphomannose isomerase — were then experimentally verified. Finally, growth experiments were performed with a D. mccartyi-containing anaerobic mixed enrichment culture to explore the effects of exogenous vitamin omission from the growth medium on D. mccartyi and the associated microbial community. The experiments showed how nutritional requirements of these bacteria changed the composition and dynamics of their associated microbial community. Overall, a systems-level approach was used in this research to obtain a fundamental and critical understanding of the metabolism and physiology of D. mccartyi in isolates, as well as in microbial communities they naturally inhabit. The results presented in this thesis, therefore, will help design effective strategies for future bioremediation efforts by D. mccartyi. iii Acknowledgements I would like to take this opportunity to thank many fascinating people who helped me complete this very long but exciting journey! It was, indeed, a life changing experience! Fisrt of all, my sincere thanks goes to my supervisors, Dr. Radhakrishnan (Krishna) Mahadevan and Dr. Elizabeth A. Edwards — both of whom are extremely caring mentors, knowledgeable scholars, and great personalities. It was their contagious enthusiasm and passion about any scientific matter, tireless inquisitive minds, and critical thinking that shaped me as a researcher during my stay at UofT. They provided me with all kinds of support and help over these many years without which this thesis wouldn’t be possible. I’m eternally grateful to both Krishna and Elizabeth for giving me such rare opportunities as to work in the amazing world of microbial metabolism. I would like to thank all past and present members of both LMSE (Laboratory for Metabolic Systems Engineering) and EdLab, including Jiao, Karthik, Bahareh, Nadeera, Nick B, Peter, Kai, Laurence, Nik, Fahime, Srinath, Pratish, Sarat, Victor, Chris, Ariel, Alison, Eve, Roya, Anna, Winnie, Max, Jennifer, Laura, Marie, Alfredo, Torsten, Jine Jine, Cheryl, Ivy, Shuiquan, Fei, Wendy, Luz, Sarah, and Olivia. These are the people with whom I shared some of the most treasured moments of my life. You are truly the most talented, enthusiastic, and beloved coworkers that I have ever worked with. I also want to express my humble gratitude to my committee members, Dr. Nicholas J. Provart and Dr. Emma R. Master. Their guidance, support, critical comments, and careful directions were some of the most influential factors that worked behind materializing this thesis. I feel fortunate to have these powerful scientific minds and fantastic personalities as my committee members. Likewise, I express my gratitude to Dr. David S. Guttman and Dr. Boris Steipe for teaching me bioinformatics, without which I wouldn’t be able to even start my research. Thanks to Dr. Alexander F. Yakunin and Dr. Alexei Savchenko for sharing your expertise in enzymology and proteomics with someone like me who is so naïve in those areas. Thanks also to Dr. Melanie Duhamel, the BioZone Assistant Director and Project Manager, for being a friend iv and “oracle” of KB-1 related challenges, as well as of monetary issues. Also, thank you to Endang Susilawati (Susie) and Angelika Duffy, the BioZone Lab Manager and Assistant Lab Manager. Susie’s motherly touch made my office-stay feel like home-stay, and Angelika’s warm support helped me steer through difficult times more easily. I am also very grateful to Anatoli Tchigvintsev and Greg Brown, the two knowledgeable technicians and biochemists, without whom my enzyme work would only be a dream! Thank you to Leticia Gutierrez and Gorette Silva for being so supportive in solving administrative matters, and always greeting with cordial smiles. Thanks to Pauline Martini and Joan Chen at the Chemical Engineering Graduate office for making the “bureaucratic part” of my graduate life easy, and providing essential information for all scholarship and funding related matters. Thanks so much to Julie Mendonca for keeping my head straight about payroll and tax related issues. Thanks also to Daniel Tomchyshyn and Weijun Gao, the Departmental and BioZone computer geeks, for providing and solving all IT supports and problems. I am truly indebted to my parents, Shamsun Nahar and Shamsul Alam, for bringing me into this spectacular world of microbes. It was their lifelong teaching, their simple yet powerful philosophies about life in general, and their intrinsic novel qualities that shaped me as a human being. Without their love, devotion, encouragement, and continuous prayers, I wouldn’t imagine to come this far. I am also extremely grateful to my parents-in-law, Shamima Ali and Mazed Ali, for their love and prayers, and most importantly, for giving me their daughter, Rutba, my wife and my eternal love. Rutba is an inspirational teacher, guide, and philosopher without whom I couldn’t even imagine to embark on this PhD journey. So, equal credit goes to Rutba on successful completion of this journey, and I dedicate this thesis to her — my best friend with whom I’m looking forward to spending many more fun-filled years. The acknowledgements remain incomplete if I don’t mention the most precious gift of my life, Manar, my daughter. Her smile and warmth of calling “Baba” refresh me every single day. Finally, I want to thank my funding agencies for their generous support during my graduate study: Government of Ontario, Genome Canada, Ontario Genomics Institute, Natural Sciences and Engineering Research Council of Canada, US Department of Defense Strategic Environmental Research and Development Program, and the University of Toronto. v Table of Contents Abstract ........................................................................................................................................... ii Acknowledgements ........................................................................................................................ iv Table of Contents ........................................................................................................................... vi List of Tables ................................................................................................................................. ix List of Figures ................................................................................................................................. x List of Appendices ........................................................................................................................ xii List of Non-Standard Abbreviations Used ................................................................................... xiv Chapter 1: Introduction ................................................................................................................... 1 1.1. Motivation ............................................................................................................................ 1 1.2. Research objectives .............................................................................................................. 3 1.3. Thesis outline ....................................................................................................................... 4 1.4. Statement of authorship and publication status .................................................................... 7 Chapter 2: General overview ........................................................................................................ 11 2.1. Systems biology ................................................................................................................. 11 2.2. Modeling microbial metabolism
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