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Doctoral Dissertation Template UNIVERSITY OF OKLAHOMA GRADUATE COLLEGE ENZYME SYSTEMS INVOLVED IN INTERSPECIES HYDROGEN AND FORMATE TRANSFER BETWEEN SYNTROPHIC FATTY AND AROMATIC ACID DEGRADERS AND METHANOSPIRILLUM HUNGATEI A DISSERTATION SUBMITTED TO THE GRADUATE FACULTY in partial fulfillment of the requirements for the Degree of DOCTOR OF PHILOSOPHY By BRYAN REGIS CRABLE Norman, Oklahoma 2013 ENZYME SYSTEMS INVOLVED IN INTERSPECIES HYDROGEN AND FORMATE TRANSFER BETWEEN SYNTROPHIC FATTY AND AROMATIC ACID DEGRADERS AND METHANOSPIRILLUM HUNGATEI A DISSERTATION APPROVED FOR THE DEPARTMENT OF MICROBIOLOGY AND PLANT BIOLOGY BY ______________________________ Dr. Michael J. McInerney, Chair ______________________________ Dr. Joseph M. Suflita ______________________________ Dr. Ralph S. Tanner ______________________________ Dr. Elizabeth A. Karr ______________________________ Dr. Michael R. Markham © Copyright by BRYAN REGIS CRABLE 2013 All Rights Reserved. I dedicate this work to my parents, Larry and Kathy Crable. Thank you for all your support and all that you have done for me. I also dedicate this work to my sister, Laura Crable. Thank you for your support and encouragement. Acknowledgements First, I need to acknowledge the intellectual and academic support of my committee chair, Dr. Michael McInerney. I also need to acknowledge two outstanding colleagues from Dr. McInerney’s group – both Neil Wofford and Dr. Jessica Sieber provided valuable technical support, training and intellectual input over the last several years. Additionally, my colleagues Dr. Housna Mouttaki, Kimberly James, Huynh Le and Dr. Johannes Kung have helped immensely with my research. Outside of Dr. McInerney’s group, I have received valuable advice and counseling from the members of my committee, Dr. Joseph Suflita, Dr. Ralph Tanner and Dr. Elizabeth Karr. Dr. Phil Klebba served as my external committee member until 2012 and provided valuable input into this research. I also thank Dr. Michael Markham, my current external committee member, for his valuable input and agreeing to join my committee so late in my program. I have also received valuable support from great colleagues here at the University of Oklahoma; among these are Dr. Chris Lyles and his wife, Laura, Chris Marks and Dr. Victoria Parisi. My colleagues at the University of California – Los Angeles, Dr. Robert Gunsalus, Dr. Lars Rohlin, Dr. Rachel Loo and Dr. Loo’s doctoral student Hong Nguyen have been instrumental in proteomic analysis. At Oak Ridge National Laboratory, Dr. Gregory Hurst was essential for completing the proteomic analysis of M. hungatei. Also, a special thank-you is due to Dr. Lisa Alvarez-Cohen and her student Xinwei Mao at the University of California – Berkley for their collaborative efforts on S. wolfei. iv I need to also thank Dr. Alfons Stams and Dr. Caroline Plugge of the University of Wageningen, the Netherlands, for allowing me to work in their group for a year. This experience was a high-point of my doctoral work, and several colleagues from Wageningen and beyond need to be thanked. Ruud Heshoff, Peer Timmers, Michael Visser and Marjet Oosterkamp all provided valuable intellectual input during my time at Wageningen. Shawn Scarlett, Dennis Rütze, Jeroen Roskam and Jeanette Smits all provided valuable assistance in navigating the complexities (and oddities) of Dutch society for a year. I thank all of them for a year of gezelligheid. Dr. Danielle Johnston, Dr. Bruce Bethke and Dr. John Stolz are all colleagues from past institutions who have continued to provide support and encouragement throughout my doctoral work. Also, I thank friends and relatives (too many to name) for all the support and encouragement over the last six years. Last, and most importantly, I need to thank my family – it’s been a long six years away from home. My parents, Larry and Kathy Crable, and sister, Laura Crable, have provided endless love, support and encouragement. I also need to acknowledge my cousin and fellow budding scientist, Jillian D’Amico – watching your intellectual growth has given me a valuable source of encouragement to keep moving forward. v Table of Contents Acknowledgements ......................................................................................................... iv List of Tables ................................................................................................................. viii List of Figures ................................................................................................................... x Preface……………………………………………………………….…………………xii Abstract ........................................................................................................................... xv Chapter 1: Summary ........................................................................................................ 1 Chapter 2: Membrane complexes formed by Syntrophomonas wolfei during axenic and syntrophic growth ............................................................................................... 10 Abstract ..................................................................................................................... 11 Introduction .............................................................................................................. 13 Materials and Methods ............................................................................................. 17 Results ……………………………………………………………………….……..30 Discussion ................................................................................................................. 58 Chapter 3: Membrane protein complexes of the syntrophic fatty and aromatic acid- oxidizing bacterium Syntrophus aciditrophicus ................................................. 67 Abstract ..................................................................................................................... 68 Introduction .............................................................................................................. 70 Materials and Methods ............................................................................................. 73 Results ……………………………………………………………….……………..84 Discussion ............................................................................................................... 118 Chapter 4: The genome and proteome of Methanospirillum hungatei strain JF1: new insights into syntrophic metabolism and biological methane production ........ 123 vi Abstract ................................................................................................................... 124 Introduction ............................................................................................................ 125 Materials and Methods ........................................................................................... 128 Results…… ............................................................................................................ 134 Discussion………………………………………………………………………....196 References .................................................................................................................... 202 vii List of Tables Table 1: Thermodynamics of butyrate, benzoate and propionate oxidation. .................. 3 Table 2: Primers for quantitative RT-PCR analysis of hydIIABC, etfAB, Swol_0698, fdhA-1, fdhA-2 and fdhA-4 in S. wolfei ........................................................................... 29 Table 3: Peptides detected from non-denaturing blue-native PAGE separation of solubilized S. wolfei membranes.. .................................................................................. 35 Table 4: Peptides detected from membrane complex testing positive for hydrogenase activity in membrane fractions of S. wolfei grown on butyrate ...................................... 51 Table 5: Peptides detected from non-denaturing blue-native PAGE separation of solubilized S. aciditrophicus membranes. ...................................................................... 88 Table 6: Specific activities of hydrogenase, formate dehydrogenase and Rnf- and Nqo- like activity in S. aciditrophicus membrane fractions.. ................................................ 103 Table 7: Specific activities of hydrogenase, formate dehydrogenase and Rnf-like activity in S. aciditrophicus membrane fractions.. ....................................................... 106 Table 8: Peptides detected from denaturing SDS-PAGE separation of S. aciditrophicus membrane fractions partially purified for Rnf-like activity. ........................................ 113 Table 9: General features of M. hungatei strain JF1 genome ...................................... 135 Table 10: Amino acid incorporation in M. hungatei strain JF1 .................................. 137 Table 11: Distribution of proteins detected from M. hungatei by functional category 147 Table 12: Core methanogenesis proteins detected from M. hungatei. ........................ 154 Table 13: Core methanogenesis proteins detected from M. hungatei only during growth butyrate-oxidizing coculture ......................................................................................... 159 viii Table 14: Peptides detected from M. hungatei showing a greater than a Log2 change of 2 increase in relative abundance in cultures from butyrate-oxidizing conditions ........ 161 Table 15: Hydrogenase proteins detected from M. hungatei ...................................... 164 Table 16: Formate dehydrogenase proteins detected from M. hungatei ..................... 168 Table 17: ATP
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