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<I>Anaeromyxobacter Dehalogenans</I>

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<I>Anaeromyxobacter Dehalogenans</I> University of Tennessee, Knoxville TRACE: Tennessee Research and Creative Exchange Doctoral Dissertations Graduate School 8-2017 Complete Denitrification yb the Non-Denitrifier Anaeromyxobacter dehalogenans: The Role of Coupled Biotic-Abiotic Reactions Jenny Rae Onley University of Tennessee, Knoxville, [email protected] Follow this and additional works at: https://trace.tennessee.edu/utk_graddiss Part of the Microbiology Commons Recommended Citation Onley, Jenny Rae, "Complete Denitrification by the Non-Denitrifier Anaeromyxobacter dehalogenans: The Role of Coupled Biotic-Abiotic Reactions. " PhD diss., University of Tennessee, 2017. https://trace.tennessee.edu/utk_graddiss/4705 This Dissertation is brought to you for free and open access by the Graduate School at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. To the Graduate Council: I am submitting herewith a dissertation written by Jenny Rae Onley entitled "Complete Denitrification yb the Non-Denitrifier Anaeromyxobacter dehalogenans: The Role of Coupled Biotic-Abiotic Reactions." I have examined the final electronic copy of this dissertation for form and content and recommend that it be accepted in partial fulfillment of the equirr ements for the degree of Doctor of Philosophy, with a major in Microbiology. Frank E. Löffler, Major Professor We have read this dissertation and recommend its acceptance: Alison Buchan, Qiang He, Karen Lloyd Accepted for the Council: Dixie L. Thompson Vice Provost and Dean of the Graduate School (Original signatures are on file with official studentecor r ds.) Complete Denitrification by the Non-Denitrifier Anaeromyxobacter dehalogenans: The Role of Coupled Biotic-Abiotic Reactions A Dissertation Presented for the Doctor of Philosophy Degree The University of Tennessee, Knoxville Jenny Rae Onley August 2017 Copyright © by Jenny R. Onley. All rights reserved. ii To Jared for your endless love and support iii Acknowledgements I would like to thank my PhD advisor, Dr. Frank Löffler, for his continued support. I appreciate his excitement for new ideas and discoveries; science can be a weary pursuit at times, and it is only through a real passion for science that we can persevere. I am grateful for the resources he provided, which stem from countless hours of hard work reading papers and writing grants. The work in this dissertation would have been impossible without him. Thank you also to Dr. Rob Sanford at the University of Illinois, who contributed ideas and patiently answered my many questions. I appreciate his thoughtful discussions and knowledgeable perspectives. There is not enough room to thank everyone who has positively impacted my time at UT. My success comes from working within a community of excellent scientists, both within and outside of my lab. Thank you to my committee members: Dr. Alison Buchan, Dr. Karen Lloyd, and Dr. Qiang He. Their thoughtful questions and suggestions greatly improved my dissertation research. Thank you to Cindy Swift, who keeps the Löffler lab running and brings a fresh perspective to our research projects. Thank you to the research assistant professors and post-doctorate fellows who have worked in the Löffler lab, including Kirsti Ritalahti, Jarrod Pollock, Silke Nissen, Gillian Walshe-Langford, Jeongdae Im, Jun Yan, Sukhwan Yoon and Devrim Kaya. Their training was indispensible and they modeled what it means to be a scientist. Thank you especially to Silke, who taught me many techniques, and who showed great patience and self-sacrifice. Her passion for training and teaching kept our lab going for a number of years, and I am grateful I had her as a mentor. Thank you to the graduate students who provided training, assistance, and excellent conversation along the way: Elizabeth Padilla-Crespo, Burcu Şimşir, Yi Yang, Meng Bi, and Nannan Jiang. And especially to Steven Higgins, my lab bench buddy, who provided valuable scientific discussions and has been an excellent sounding board for my ideas. Thank you to Samiha Ahsan, my undergraduate mentee, whose contributed her time and ideas to my project and provided a cheerful and encouraging presence in the lab. Thank you to the rest of the Löffler lab, both past and present members; you all contributed to the team and I am grateful I was a part of it. Thank you to Dr. Jeffrey Becker and the rest of the faculty who provided thoughtful comments on my projects over the years. A unique quality of our department iv is our close connection with the Oak Ridge National Laboratory, and I am grateful for our collaborators and colleagues at ORNL as well (especially Dr. Chris Schadt, who allowed me to do a rotation in his lab). Thank you as well to my fellow graduate students in the Microbiology department who have provided stimulating scientific conversation and support. They are too many to name but I truly appreciate the community of scientists at UT. A special thanks to Samantha Coy and Pooja Saraf Dogra, who really took care of me the last two years of graduate school and are beautiful ladies, inside and out. I am grateful to Steven Higgins, Samiha Ahsan, and Ashley Frank for their suggestions and revisions of my dissertation. A special thanks to Steven and also Luis Orellana at the Georgia Institute of Technology, who patiently helped me sharpen my bioinformatic skills. I am also grateful for the funding agencies that supported my research, especially the US Department of Energy Genomic Science Program (Award DE-SC0006662). Thank you to my family as well: Mom, Dad, Holly, Mandy, and Devon. You kept me grounded and encouraged me. Special thanks to Mom and Dad, for cultivating my love of science and helping me to pursue my dreams. They saw the spark when I was young, and fanned it into a flame. Finally, I would like to thank my husband, Jared Onley. He has shown me faithful love and support through the ups and downs of graduate school. He believed in me though the entire process. During his own arduous trek through medical school and residency, he continued to sacrifice his time and energy and support me. It has been rewarding to have a scientifically minded husband with whom to share my exciting discoveries (as well as an abundance of boring details). I am eternally grateful to my supporter and cheerleader. v Abstract Nitrous oxide (N2O) is a potent greenhouse gas and ozone-depleting substance produced by many different pathways in the nitrogen cycle, including nitrification, denitrification, and chemodenitrification. Abiotic sources of N2O such as the chemical - reaction between nitrite (NO2 ) and ferrous ion (Fe[II]) are generally neglected in studies - of N turnover in soils. Abiotic controls containing nitrate (NO3 ) and ferric iron (Fe[III]) - fail to capture potential reactions between intermediates of N cycle pathways (e.g., NO2 - + as an intermediate in NO3 reduction to ammonium [NH4 ] or nitrogen gas) or replenishment of reactants by iron cycling. Recent studies suggest that Fe(II) plays an important role in N turnover through combined biotic and abiotic reactions. Anaeromyxobacter dehalogenans strain 2CP-C is a common soil bacterium with a versatile metabolism, including microaerobic and anaerobic respiration. A. dehalogenans - + reduces Fe(III) to Fe(II) and reduces NO3 to NH4 via respiratory ammonification. The present work investigates the mechanisms by which A. dehalogenans utilizes O2 and the - synergistic effects of Fe(III) and NO3 reduction. Evidence for respiration of 21% O2 via a low-affinity cytochrome c oxidase is presented, further expanding the respiratory versatility of A. dehalogenans. A previously unrecognized ecophysiological role is - revealed in which A. dehalogenans reduces NO3 to approximately 50% N2 and 50% + NH4 via coupled biotic-abiotic reactions, revealing a mechanism for denitrification in - the absence of nitric oxide (NO)-forming NO2 reductases. Further analysis of publicly available sequenced genomes reveal other microorganisms with the potential to couple - - biotic-abiotic reactions for reduction of NO3 to N2 in the absence of NO-forming NO2 reductases. Finally, the effects of sulfide and molybdenum are tested, demonstrating that - + - A. dehalogenans reduces NO3 to NH4 and NO2 to N2O in the presence of Fe(II) and - sulfide, due to the inhibition of NO3 and N2O reductases by sulfide sequestration of trace metals. Collectively, this work demonstrates an underestimated mechanism for denitrification and expands our knowledge of the role of A. dehalogenans in O2 respiration and Fe and N cycling. Future efforts assessing the fate of N in agricultural soils should take into account the iron, molybdenum, and sulfide content of soils in addition to molecular information. vi Table of Contents Chapter 1: Introduction .................................................................................................... 1 Background ................................................................................................................................ 2 The nitrogen cycle ................................................................................................................... 2 The iron cycle .......................................................................................................................... 4 Anaeromyxobacter: A unique member of Myxococcales .......................................................
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