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Ucalgary 2017 Toth Courtney.Pdf University of Calgary PRISM: University of Calgary's Digital Repository Graduate Studies The Vault: Electronic Theses and Dissertations 2017 Characterizing and Accelerating Methanogenic Hydrocarbon Biodegradation Toth, Courtney Toth, C. (2017). Characterizing and Accelerating Methanogenic Hydrocarbon Biodegradation (Unpublished doctoral thesis). University of Calgary, Calgary, AB. doi:10.11575/PRISM/25297 http://hdl.handle.net/11023/3980 doctoral thesis University of Calgary graduate students retain copyright ownership and moral rights for their thesis. You may use this material in any way that is permitted by the Copyright Act or through licensing that has been assigned to the document. For uses that are not allowable under copyright legislation or licensing, you are required to seek permission. Downloaded from PRISM: https://prism.ucalgary.ca UNIVERSITY OF CALGARY Characterizing and Accelerating Methanogenic Hydrocarbon Biodegradation by Courtney Rose Afton Toth A THESIS SUBMITTED TO THE FACULTY OF GRADUATE STUDIES IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY GRADUATE PROGRAM IN BIOLOGICAL SCIENCES CALGARY, ALBERTA JULY, 2017 © Courtney Rose Afton Toth 2017 Abstract Microbial transformation of hydrocarbons to methane is an environmentally relevant but slow process taking place in a wide variety of electron acceptor-depleted environments, from oil reservoirs and coal deposits, to contaminated groundwater and deep sediments. Despite the prevalence of chemical evidence demonstrating methanogenic hydrocarbon metabolism in field investigations, there are significant gaps in our understanding of the anaerobic activation mechanisms of model substrates (particularly monoaromatic and polycyclic aromatic hydrocarbons, PAHs) and whole crude oil, as well as the degradation pathways and microorganisms governing oil transformation to methane. By studying the chemical and functional responses of methanogenic consortia to enrichment on model and mixed hydrocarbon substrates, we can gain a more complete understanding of the fate of hydrocarbon components in electron acceptor-depleted environments. In this dissertation, we sought to characterize the biodegradation of an expanded range of hydrocarbon substrates using a series of chemical and molecular approaches. We also explored cultivation-based strategies for optimizing rates of methanogenic hydrocarbon utilization, of which the most successful methods were adopted for future cultivation studies described here. Members of the Desulfosporosinus genus, known to catalyze methanogenic toluene biodegradation, were also found to co-metabolize other alkylbenzene substrates. Other members of the Firmicutes phylum, such as Desulfotomaculum, were shown to be functionally capable of activating toluene by addition to fumarate in a crude oil-degrading produced water consortium, and are proposed to play a key role in the formation of heavy oil in petroleum reservoirs. Microbial community sequencing, DNA-based stable isotope probing, and metagenomic surveys of previously established and novel methanogenic PAH- degrading cultures suggest that Clostridium may be important for degrading larger aromatic ii structures by an unknown mechanism. Experimental evidence of a hypothetical energy conservation mechanism in Syntrophus was detected during alkylbenzene biodegradation, suggesting this organism plays a vital role in coordinating syntrophic hydrocarbon biodegradation in a bioenergetically favourable manner. In all, this research has gleaned new insights into the microorganisms and metabolic processes regulating methanogenic hydrocarbon biodegradation, and has produced a wealth of new research questions to be explored in future investigations. iii Acknowledgements I find it surreal having reached the end of my graduate student career. Admittedly, I had grown quite content living day by day as a perpetual student, with no real concern for the future. As I reflect upon these past years, however, I find comfort in knowing that I have all the tools I need to dive into the next chapter of my life head-first, ready and eager, and will always have the support of a close-knit group of friends, family and colleagues. As cliché as it sounds, I struggle to find words expressing my gratitude. I begin by offering my sincerest thanks to my supervisor, mentor, and friend, Dr. Lisa Gieg. I am truly inspired by everything you do. Though I will always credit you for helping me reach my (academic) potential, perhaps more importantly, your guidance has also helped to remind me to live life to the fullest. Thank you to my supervisory committee members Dr. Gerrit Voordouw and Dr. Peter Dunfield for your invaluable advisement and assessment of my doctoral research, and to my external examiners Dr. Elizabeth Edwards and Dr. Steve Larter for your thoughtful feedback that has helped to improve this dissertation. Also, thank you to Dr. Marc Strous and Dr. Douglas Storey for chairing my candidacy examination – I learned more about myself in those few weeks than I had in as many years. To the aptly named ‘Giegers,’ past and present, thank you for enriching my graduate student experience with your warmth and wisdom. To the latter, I ask that you continue the traditions of laboratory shenanigans (in a safe manner) and to welcome incoming lab members with open arms. I’d like to give special recognition to Dr. Jane Fowler, Dr. Carolina Berdugo-Clavijo, and Dr. Sandra Wilson, who patiently trained and supported me throughout my graduate studies – you are the real MVPs and friends for life. I would also like to personally recognize and thank former student-turned-technician Corynne O’Farrell for her outstanding contributions supporting my research. Thank you to the Petroleum iv Microbiology Research Group, the Energy Bioengineering and Geomicrobiology Research Group, and the research team of Dr. Peter Dunfield for your mentorship and comradery during my graduate studies – it has been an absolute pleasure working and collaborating with you. To Jaspreet and Jessica, I am so proud of the women you’ve become and am forever grateful for having taken this journey through graduate school with you. To my dearest friend Lindsay – thank you for your unwavering friendship, your endless enthusiasm, and for always having time for tea. To Sean, Iain, and all patrons of ‘Whiskey Friday,’ I can’t thank you enough for all the laughs and adventures we’ve shared, and I hope there are more to come. Last, but first in my heart, thank you to my family who fostered my sense of wonder and for supporting me through many, many, years of post-secondary education. Cameron and Al – I couldn’t have done this without you. v Dedication For Lisa, Great leaders don’t tell you what to do; They show you how it’s done. vi Table of Contents Abstract ............................................................................................................................... ii Acknowledgements ............................................................................................................ iv Dedication .......................................................................................................................... vi Table of Contents .............................................................................................................. vii List of Tables .................................................................................................................... xii List of Figures and Illustrations .........................................................................................xv List of Symbols, Abbreviations and Nomenclature ........................................................ xxii Epigraph ......................................................................................................................... xxiv CHAPTER ONE: LITERATURE REVIEW .......................................................................1 1.1 Introduction ................................................................................................................1 1.2 Bioenergetic considerations of anaerobic hydrocarbon biodegradation ....................3 1.3 Methanogenic hydrocarbon biodegradation – An overview ......................................6 1.4 Pathways of anaerobic hydrocarbon biodegradation ...............................................13 1.4.1 Initial activation mechanisms ..........................................................................13 1.4.1.1 Fumarate addition ..................................................................................13 1.4.1.2 Hydroxylation ........................................................................................15 1.4.1.3 Carboxylation .........................................................................................17 1.4.1.4 Methylation ............................................................................................19 1.4.2 Pathways following initial activation ..............................................................20 1.5 Tools for assessing anaerobic hydrocarbon biodegradation ....................................21 1.5.1 Geochemical monitoring .................................................................................22 1.5.2 Hydrocarbon metabolite analysis ....................................................................23 1.5.3 Molecular microbial analysis ..........................................................................25 1.5.4 Biodegradative gene analysis ..........................................................................27
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