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Biological Mechanisms of Uranium Transformation Catalyzed by Geobacter Bacteria

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Biological Mechanisms of Uranium Transformation Catalyzed by Geobacter Bacteria BIOLOGICAL MECHANISMS OF URANIUM TRANSFORMATION CATALYZED BY GEOBACTER BACTERIA By Dena L. Cologgi A DISSERTATION Submitted to Michigan State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Microbiology and Molecular Genetics 2012 ABSTRACT BIOLOGICAL MECHANISMS OF URANIUM TRANSFORMATION CATALYZED BY GEOBACTER BACTERIA By Dena L. Cologgi An insufficient knowledge of the biological mechanisms of contaminant transformation often limits the performance of in situ subsurface bioremediation and long-term stewardship strategies. The in situ stimulation of Fe(III) oxide reduction by Geobacter bacteria leads to the concomitant precipitation of U(VI) from groundwater. However, the biological mechanism behind this reaction has remained elusive. Because Fe(III) oxide reduction requires the expression of conductive pili in Geobacter, we also evaluated their contribution to uranium reduction. In chapter 2 of my dissertation I demonstrate a previously unrecognized role for Geobacter pili in the extracellular reduction of uranium and its essential function as a catalytic and protective cellular mechanism. The expression of pili by Geobacter also promotes cell aggregation and biofilm formation. Recent work has shown that Geobacter cells transition from planktonic to biofilm physiologies during the active phase of U reduction in the subsurface. Despite these findings, the contribution of Geobacter biofilms to uranium removal and reduction has not been investigated. In chapter 3 of my dissertation I demonstrate that multilayer biofilms are able to reduce and tolerate substantially more U than planktonic cells for prolonged periods of time, making them an attractive option for the development of permeable biobarriers for U bioremediation. I also demonstrate the role of pili as a primary U reductase in the biofilm. To gain further insight into how biofilms transform U, in chapter 4 of my dissertation I screened a library of transposon-insertion mutants and identified mutants with biofilm defects. This study confirmed the role of Geobacter pili in biofilm formation, and identified other genes encoding cell envelope and electron transport components that had not previously been implicated in biofilm development. These molecular markers can be used to predict and monitor the physiological state of Geobacter bacteria during the in situ bioremediation of U. Previous work, including the prior chapters of my dissertation, has highlighted the importance of the cell envelope and its components for the survival of Geobacter in the subsurface. However, little is known regarding the regulation of the cell envelope. Thus, I investigated the role of the Geobacter’s ECF sigma factor, RpoE. In the last chapter of my dissertation, I show that RpoE is required for response to cell envelope stress, as well as the regulation of Geobacter’s extracellular electron transfer pathways. This highlights the functional specialization that RpoE has undergone to control the adaptive responses that enable Geobacter bacteria to survive in the environment, and links my findings to the physiology of Geobacter in the subsurface. DEDICATION This dissertation is dedicated to my family. Thank you for staying rational when I wasn’t, and believing in me when I didn’t. I am so fortunate to have you in so many ways. I am incredibly thankful that being in Michigan has given me the opportunity to know my family in New York and become a part of their lives, especially during this past year. Thank you for all of your love, guidance and support. iv ACKNOWLEDGEMENTS I would first like to acknowledge my mentor, Dr. Gemma Reguera, who has been there for me throughout this process and taught me more than I can describe. Thank you for taking a tremendous risk and entrusting your first lab to two very enthusiastic (but even more inexperienced and naive!) first-year rotation students. I am proud to have been a part of that beginning. I also need to extend a huge thank you to Allison Speers who has been with me since day one when we started the transposon mutagenesis together during our rotation. I don’t think I would have survived grad school without you, Allison – literally! I will always owe you for accompanying me to Argonne and ensuring I didn’t do something horrible (hitting the big red button, locking myself in the hutch, blowing up the synchrotron...) during those late-night sample changes performed in a nearly non-functional, sleep-deprived state. I would also like to thank the other individuals who contributed directly to the work presented in my dissertation. Blair Bullard worked side-by-side with me on many of the biofilm experiments, and was instrumental in obtaining anything and everything needed for my research! Two amazing undergrad students, Annie Otwell and John Rotondo worked with me on the transposon mutagenesis project. Annie and John, you made my first experiences mentoring both easy and fun; I was very lucky to have you. No one else in the world would have so calmly tolerated my ups and downs, or endured so well the endless colony picking, plate transfers, and rarely-successful sequencing attempts. I would also like to acknowledge Sanela Lampa-Pastirk, who developed the pili isolation protocol used in chapter 2. Sanela welcomed v me into her family and provided significant support for me, both emotionally as well as scientifically, throughout this process. I would like to thank our collaborator, Shelly Kelly (EXAFS analysis) not only for her scientific contributions, but also for taking the time to train (and in general put up with) Allison and me so we could play a more active role in our trips to Argonne. And special thanks for being such a wonderful hostess and humoring us in our non-scientific adventures including the search for albino deer, the tricycle rides, and the hunt for the coffee cart! I’d also like to acknowledge the rest of the Sector 20 staff at Argonne National Lab for all of their help and patience Acknowledgement must also go to the other members of the Reguera Lab who may not have been directly involved in my research, but have had a huge impact nonetheless. First, to my long-term lab-mates Jenna Young, Becky Steidl, and Mike Manzella, along with Allison and Sanela -- what can I say? I can’t imagine a lab without you. You have truly been like family. Thank you so much for your humor, support and loyalty. I would never have survived without you. I would also like to thank Bryan Schindler, Jihwan Hwang, Ana Lara, and Catherine Silva. Though they were in our lab only a short time, I am very thankful for both their scientific input and conversations about life. I have to especially thank Ana for keeping me company during those depressing late night battles with the KPA! I would also like to acknowledge our dishwashers and media-makers (Marvin, Max, Derek, Mike2, Mellissa, Karl, Katie, Alex and Eric). Without them our lab couldn’t function. The last in this category is Kwi Kim, who has relentlessly kept me on track and made sure that I didn’t forget what’s important in life. Other people who have been integral to the success of my grad school career include my committee members, Dr. Rob Britton, Dr. Terry Marsh, and Dr. Lee Kroos, who have been vi very patient and supportive throughout this process. I would also like to acknowledge several individuals who assisted with some of the technical aspects of my research including Matthew Marshall (PNNL), Evgenya Shelobolina (University of Wisconsin-Madison) and Kazem Kashefi, who provided some of the protocols crucial to my work, as well as Weimin Chen (and Sanela and Igor) who helped me master the KPA. I would also like to extend a huge thank you to the amazing people at the Center for Advanced Microscopy (Alicia Pastor, XouDong Fan, Melinda Frame, Carole and Stanley Flegler) who have gone out of their way to be helpful, and were always understanding when I was running very late! As Alicia (who I also need to thank for being such a great friend and neighbor!) once so eloquently put it, “this is the Center for Advanced Microscopy, where all your dreams come true!” I have been fortunate enough to have been funded throughout my Ph.D. by agencies such as the National Institute of Environmental Health Science’s Superfund program (R01 ES017052-03), the Office of Science (BER), U.S. Department of Energy (DOE) (DE-SC0000795), the College of Natural Science at Michigan State University (Hensley fellowship), and the Biogeochemistry Environmental Research Initiative at Michigan State University (research fellowship). PNC/XSD facilities and research at the APS are supported by the US DOE-BES, a Major Resources Support grant from NSERC, the University of Washington, Simon Fraser University and the APS. The APS is an Office of Science User Facility operated for the U.S. DOE’s Office of Science by Argonne National Laboratory and supported by the U.S. DOE under contract No. DE-AC02-06CH11357. vii I, of course, also have to acknowledge the other MMG grad students who have been with me over the years. I am incredibly grateful for your camaraderie, companionship, support and scientific advice, and I wish you all the best. Lastly, I would like to thank my family, to whom this dissertation is dedicated. viii TABLE OF CONTENTS LIST OF TABLES .......................................................................................................... xii LIST OF FIGURES ....................................................................................................... xiii KEY TO SYMBOLS
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