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Thesis Abstarctand Table of Contents, Jan 8, 2012 Microorganisms and Metabolic Pathways Involved in Anaerobic Benzene Biodegradation under Nitrate-Reducing Conditions By Roya Gitiafroz A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Graduate Department of Chemical Engineering and Applied Chemistry University of Toronto !Copyright by Roya Gitiafroz (2012) Microorganisms and Metabolic Pathways Involved in Anaerobic Benzene Biodegradation under Nitrate-Reducing Conditions Doctor of Philosophy, 2012, Roya Gitiafroz Chemical Engineering and Applied Chemistry, University of Toronto Abstract This thesis describes the characterization of benzene-degrading denitrifying cultures. Four objectives were pursued. The first objective was to identify conditions that promote or inhibit benzene decomposition and thus, to improve the biodegradation capacity of the cultures. FeS, resazurin, and nitrite had a detrimental impact on benzene degradation, whereas addition of supernatant from an active culture improved the benzene degradation activity by reducing the lag times. The second objective was to determine the microbial community composition in enrichment cultures and to identify the bacterial species that mediate benzene mineralization. Five dominant bacterial Operational Taxonomic Units (OTUs) were identified. The most abundant phylotype was related to the gram-positive Peptococcaceae family. Other bacteria present were closely affiliated with Dechloromonas, Azoarcus, Chlorobi and Anammox species. To correlate the growth of these specific microbes with benzene degradation, the abundance of specific 16S rRNA genes was monitored during mineralization process using quantitative polymerase chain reaction (qPCR). Based on the result of qPCR experiments and information about the metabolisms of the above bacteria, a syntrophic mode of benzene degradation was hypothesized to occur under denitrifying conditions. In this process, Peptococcaceae initiate attack on benzene, and ferment benzene to hydrogen and low molecular weight products such as acetate. ii These products are then consumed by nitrate-respiring Azoarcus and Dechloromonas or phototrophic Chlorobi. Anammox bacteria recycle and detoxify nitrite, and stabilize the culture. The third objective was to isolate and characterize pure cultures with the ability to mineralize benzene anaerobically. Dechloromonas- and Dechlorosoma-like microorganisms were isolated from several benzene-degrading microcosms. Theses bacteria, however, were not able to metabolize benzene anaerobically. The fourth objective was to investigate the key metabolic steps in the anaerobic benzene degradation pathway and to identify enzymes that are involved in this process. Differential transcription during growth of the culture on benzene versus growth on a metabolite of benzene degradation, i.e. benzoate was examined. Carboxylase-related genes were specifically transcribed in the presence of benzene. Furthermore, mRNA sequences corresponding to the genes that encode different enzymes of the benzoyl-CoA degradation pathway were present in the culture. These findings suggest that mineralization of benzene starts by its activation to benzoate through a carboxylation reaction catalyzed by benzene carboxylase. Benzoate is further metabolized through benzoyl-CoA pathway. iii Acknowledgements I like to thank my supervisor Prof. E. A. Edwards and express my most sincere gratitude for her enthusiasm, patience, and support during this research. Her passion for research and life provided me with motivation and inspiration throughout this work. I like to thank Prof L. Raskin for accepting me as a member of her research group and providing me with the guidance throughout this study. I also would like to thank her for always being there for me. I like to thank my other thesis committee members: Prof. G. Allen and Dr. D. Major for their advice and guidance in all steps of this study. I like to thank Prof. P. Adriaens for allowing me to use his lab facility. I like to thank my colleagues in Edwards’ and Raskin’s Labs. This study was made possible by the financial support of Natural Sciences and Research Council of Canada, Ontario Graduate Scholarship, and the Graduate School of Chemical Engineering and Applied Chemistry at University of Toronto. I especially like to thank my Husband Dr. Hossein Tavana and my parents Zahra Ghaffari and Mohammad Hossein Gitiafroz for their love, support, and patience. This thesis is dedicated to my family. iv Table of Contents Abstract......................................................................................................................................... ii Acknowledgements .................................................................................................................. iv Table of Contents ........................................................................................................................v List of Tables................................................................................................................................x List of Figures ........................................................................................................................... xii Nomenclature ........................................................................................................................... xiv Chapter 1: Introduction and Objectives.................................................................................1 1.1. Introduction ..................................................................................................................2 1.1.1. Benzene: a groundwater contaminant ...........................................................2 1.1.2. Benzene bioremediation.................................................................................2 1.2. Research objectives.......................................................................................................4 1.3. Thesis outline................................................................................................................6 1.4. References Chapter 1 ....................................................................................................7 Chapter 2. Background and Literature Review .................................................................12 2.1. Background.................................................................................................................13 2.1.1. Bacterial energetics and growth...................................................................13 2.2. Literature review.........................................................................................................16 2.2.1. Aerobic benzene degradation.......................................................................16 2.2.2. Anaerobic benzene degradation...................................................................19 2.3. Syntrophic mineralization of benzene ........................................................................33 2.4. Conclusions.................................................................................................................35 2.5. References Chapter 2 ..................................................................................................36 Chapter 3: Maintenance and Optimization of Growth of Benzene-Degrading Nitrate-Reducing Enrichment Cultures ...............................................................................45 3.1. Introduction.................................................................................................................46 3.2. Materials and Methods................................................................................................47 3.2.1. Maintenance of benzene-degrading nitrate-reducing enrichment cultures..47 3.2.2. Nitrite removal.............................................................................................48 3.2.3. Medium omission and addition experiments ...............................................48 v 3.2.4. Analytical methods ......................................................................................49 3.3. Results and discussion ................................................................................................49 3.3.1. Monitoring benzene degradation and nitrate reduction in enrichment cultures...................................................................................................................49 3.3.2. Preventing nitrite accumulation and inhibition............................................51 3.3.3. The effect of different components of medium on the lag time ..................53 3.4. Conclusions.................................................................................................................64 3.5. Recommendations for future work .............................................................................64 3.6. References Chapter 3 ..................................................................................................67 Chapter 4: Multiple Syntrophic Associations in Nitrate-Reducing Benzene- Degrading Cultures ..................................................................................................................70 4.1. Introduction.................................................................................................................71 4.2. Materials and Methods................................................................................................74 4.2.1. Benzene-degrading nitrate-reducing cultures and subcultures ....................74
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