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Evidence for Perchlorate-Coupled Molybdenum and Nickel Carbon Monoxide Dehydrogenase CO Oxidation and Characterization of Novel Perchlorate-Reducing Haloarchaea

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Evidence for Perchlorate-Coupled Molybdenum and Nickel Carbon Monoxide Dehydrogenase CO Oxidation and Characterization of Novel Perchlorate-Reducing Haloarchaea Louisiana State University LSU Digital Commons LSU Doctoral Dissertations Graduate School 5-21-2021 Evidence for Perchlorate-Coupled Molybdenum and Nickel Carbon Monoxide Dehydrogenase CO Oxidation and Characterization of Novel Perchlorate-Reducing Haloarchaea Marisa Russell Myers Louisiana State University and Agricultural and Mechanical College Follow this and additional works at: https://digitalcommons.lsu.edu/gradschool_dissertations Part of the Biology Commons, and the Environmental Microbiology and Microbial Ecology Commons Recommended Citation Myers, Marisa Russell, "Evidence for Perchlorate-Coupled Molybdenum and Nickel Carbon Monoxide Dehydrogenase CO Oxidation and Characterization of Novel Perchlorate-Reducing Haloarchaea" (2021). LSU Doctoral Dissertations. 5555. https://digitalcommons.lsu.edu/gradschool_dissertations/5555 This Dissertation is brought to you for free and open access by the Graduate School at LSU Digital Commons. It has been accepted for inclusion in LSU Doctoral Dissertations by an authorized graduate school editor of LSU Digital Commons. For more information, please [email protected]. EVIDENCE FOR PERCHLORATE-COUPLED MOLYBDENUM AND NICKEL CARBON MONOXIDE DEHYDROGENASE CO OXIDATION AND CHARACTERIZATION OF NOVEL PERCHLORATE-REDUCING HALOARCHAEA A Dissertation Submitted to the Graduate Faculty of the Louisiana State University and Agricultural and Mechanical College in partial fulfillment of the requirements for the degree of Doctor of Philosophy in The Department of Biological Sciences by Marisa Russell Myers B.S., Louisiana State University, 2014 August 2021 ACKNOWLEDGEMENTS I want to thank my mentor and chair of my dissertation committee, Dr. Gary King for first welcoming me into the lab as a young undergraduate and guiding me throughout both my Bachelor and Doctoral programs. His leadership and engagement made these projects possible and successful. I would also like to thank my committee members, Dr. Gregg Pettis, Dr. William Doerrler, and former committee members Dr. J. Cameron Thrash, Dr. Brent Christner, and Dr. Yuchen Liu for their thoughtful guidance and feedback. I also thank the current and former members of the King lab, Dr. Caitlin King, Craig Judd, Dr. Shannon McDuff Johnson, Amber DePoy, and Eric Martinez for your mentoring, feedback, and support. To my friends, Kristen Campbell, Lindsey Morphis, Reagan Dugan, Scott Grimmell, Katie Rose DeLeo, Andrew McGuffey, Charles Zimmerman, Grigor Sargsyan, Aheli Mukerji, Wesley Morgan, Emily Morgan, David Alspaugh, and Frederic Marazzato, thank you for always listening, giving feedback, providing endless encouragement and laughs, and reminding me it is ok to leave the lab and have a solid climbing send session. I can truly say I wouldn’t have been as happy and motivated without ya’ll in my life. To my family, Marion, Lisa, and Marty, thank you for your love, support, and teaching me hard work, without which no graduate student can be successful. To my in-laws, Douglas, Florence, Daniel, Katie, and little Addison, thank you for welcoming, supporting, and loving me as one of your own. Finally, I am eternally grateful for my husband, David Myers. I could not have done this without you, you have shown me strength, commitment, graciousness, and leadership which allowed our friendship and marriage to thrive after nearly seven years of long distance. You remind me every day to not give up, support me in my choices, and encourage me in my goals. ii This research was funded by the US National Science Foundation award EAR-15654499, and NASA awards NNX15AE82A, and 15-EXO15_2-0147. iii TABLE OF CONTENTS Acknowledgements .................................................................................................................... ii Abstract ....................................................................................................................................... v Chapter 1. Introduction ............................................................................................................... 1 Chapter 2. Perchlorate-Coupled Carbon Monoxide (CO) Oxidation: Evidence for a Plausible Microbe-Mediated Reaction in Martian Brines ....................................................... 19 Chapter 3. Addendum: Perchlorate-Coupled Carbon Monoxide (CO) Oxidation: Evidence for a Plausible Microbe-Mediated Reaction in Martian Brines ................................................ 36 Chapter 4. Halobacterium bonnevillei sp. nov., Halobaculum saliterrae sp. nov., and Halovenus carboxidivorans sp. nov., three novel carbon monoxide-oxidizing Halobacteria from saline crusts and soils ....................................................................................................... 42 Chapter 5. Halanaeroarchaeum oxyrespirans sp. nov., a novel oxygen-respiring, perchlorate-reducing extreme halophile .................................................................................. 59 Chapter 6. Perchlorate-Coupled Carbon Monoxide (CO) Oxidation in Moorella glycerini: A Novel Mechanism for Nickel-Dependent Carbon Monoxide Dehydrogenases ................... 83 Chapter 7. Conclusions and Future Directions ........................................................................ 92 Appendix A. Supplementary Material for Chapter 2 ................................................................ 96 Appendix B. Supplementary Material for Chapter 4 ................................................................ 99 Appendix C. Supplementary Material for Chapter 5 .............................................................. 103 Appendix D. Permission to Reproduce Chapters 2 and 3 ....................................................... 107 Appendix E. Permission to Reproduce Chapter 4 .................................................................. 109 References ............................................................................................................................... 111 Vita ......................................................................................................................................... 126 iv ABSTRACT Carbon monoxide (CO) has been exploited as a microbial energy source for much of life’s evolutionary history. A phylogenetically diverse array of microorganisms can oxidize CO using two distinct CO dehydrogenases, molybdenum-dependent (Mo-CODH) and nickel- dependent (Ni-CODH). Aerobes and facultative organisms contain Mo-CODHs which allow them to utilize oxygen as an electron acceptor in addition to alternatives such as nitrate and sulfate. Obligate anaerobic organisms contain Ni-CODHs, which oxidize CO at elevated concentrations, but cannot utilize oxygen. In systems where organic matter deposits are limited or absent, atmospheric trace gases such as CO are thought to assist in supporting the growth and survival of microbial communities. Extraterrestrially, the Martian atmosphere is dominated by CO2, however, CO also has also been documented at substantial levels. Martian regolith contains only trace levels of organic carbon, leaving CO as potentially the most abundant and available substrate capable of supporting near-surface microbial activity. However, Martian regolith also contains perchlorate, while potentially toxic it also serves an abundant potential oxidant. At locations such as the recurrent slope lineae, hypersaline perchlorate-based brines are thought to exist. Though previously unexplored for CO oxidation, chlorine oxyanions may act as suitable electron acceptors, expanding the current range of both Mo-CODH and Ni-CODH CO oxidizing microorganisms. This study used a variety of culture-dependent approaches, cultivating four novel haloarchaea from the Bonneville Salt Flats and surrounding saline soils capable of utilizing - CO, ClO4 , or a metabolic coupling. Halovenus carboxidivorans was capable of CO oxidation, while Halobacterium bonnevillei and Halobaculum saliterrae, represent the first microbes - capable of perchlorate-coupled CO oxidation at concentrations up to 1 M ClO4 . All three isolates contained Mo-CODHs. The provisional species, Halanaeroarchaeum oxyrespirans, is v capable of growth via perchlorate reduction, independently of nitrate, a first for haloarchaeal cryptic perchlorate reduction. Additionally, H. oxyrespirans, can respire oxygen, expanding the known capacities of the genus. Perchlorate-coupled CO oxidation was further expanded to include carboxidotrophic Ni-CODH containing microbes by using the thermophilic Firmicute Moorella glycerini DSM 11254T as a model organism. Collectively, the isolation of these haloarchaeal cultivars contributed to the expansion of haloarchaeal diversity through both physiological and genomic characterization. vi CHAPTER 1. INTRODUCTION Microbes have exploited various anaerobic metabolic processes for energy since the origin of life. Carbon monoxide (CO), the second most common molecule in the universe, has contributed to diverse and significant processes throughout the history of terrestrial life (Aylward and Bofinger, 2001; Miyakawa et al., 2002; King and Weber, 2007). Life on Earth is likely to have exploited CO for much of its evolutionary history, including possible early chemolithotrophs near anoxic hydrothermal vent systems (Svetlichny et al., 1991; Sokolova et al., 2004). In the absence of organic matter deposits, atmospheric trace gases such as CO may aid in supporting the growth and survival of microbial communities (King, 2003; King et al., 2008). Microbial carbon monoxide oxidation is known to proceed under both aerobic and
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