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ABSTRACT ZELDES, BENJAMIN. Leveraging Extreme ABSTRACT ZELDES, BENJAMIN. Leveraging Extreme Thermoacidophily for Archaeal Metabolic Engineering (Under the direction of Dr. Robert Kelly). Recent improvements in molecular genetics tools for extreme thermophiles mean that microbial metabolic engineering is now possible at temperatures in excess of 70°C. Thermophilic organisms have had a dramatic impact in both science and industry based on the utility of their thermostable, thermoactive enzymes. Extreme thermophile metabolic engineering means that more complex bio-transformations involving multi-enzyme pathways are now possible. Among the many promising microorganisms for industrial biotechnology are members of the thermoacidophilic (Topt > 75°C, pHopt < 3) archaeal order Sulfolobales, many of which are chemolithoautotrophs. As such, they contain pathways for acquiring energy from inorganic chemical sources, such as metal ores and elemental sulfur, and a carbon fixation cycle for taking up CO2. Portions of the carbon fixation cycle expressed in another extreme thermophile, Pyrococcus furiosus, have produced the bioplastic precursor 3-hydroxypropionate (3HP), where one-third of the carbon in the final product is derived from CO2. Expression of chemical production pathways within a chemolithoautotrophic species of Sulfolobales would allow for production of carbon chemicals entirely from carbon dioxide, using inorganic chemical energy sources which are plentiful and inexpensive. Metabolic engineering also has the potential to provide insights into aspects of thermophilic metabolism that remain poorly understood. Co-expression of additional enzymes alongside those for carbon fixation in P. furiosus determined that carbonic anhydrase plays an important role in CO2 uptake in the Sulfolobales, and a biotinylating maturation enzyme dramatically improved function of the first enzyme in the cycle. Similar insights into the process of sulfur oxidation in Sulfolobales were obtained by cloning two sulfur oxidation enzymes into Sulfolobus acidocaldarius, a species in which lithoautotrophic sulfur oxidation has been lost. While the sulfur oxygenase reductase (SOR) and thiosulfate quinone oxidoreductase (TQO) had been characterized individually, their co-expression revealed cooperative effects as a full sulfur oxidation pathway. Sulfur was toxic to the strain expressing SOR alone, but adding TQO led to robust growth in the presence of sulfur and significant sulfur oxidation. Transcriptomic analysis revealed that S. acidocaldarius retains mechanisms to detect and respond to the presence of sulfur, but exhibits minimal response to CO2. Future work will focus on a carbon-fixation associated regulatory system, and the new model species for sulfur oxidation, Acidianus brierleyi, for which a genome sequence has just become available, and sulfur-transcriptome data is pending. Continued progress in extreme thermophile metabolic engineering will depend on fully realizing the unique advantages found at high temperatures. One of the most promising is the potential for facilitated purification and continuous removal of a volatile chemical as it is produced by a thermophilic host, termed “bio-reactive distillation” (BRD). Acetone has both the requisite volatility, and value as a chemical product. Moderately thermophilic acetone production has been demonstrated, but BRD requires temperatures in excess of 70°C. Despite a dearth of thermophilic native acetone producers, enzyme candidates were identified, including the first thermophilic acetoacetyl-CoA-transferases to be characterized, and an unusually thermostable enzyme from the mesophile Clostridium acetobutylicum. The isolated subunits of CoA transferase exhibit dramatically different thermostabilities, but in complex alpha protects the more labile beta. Together with a previously characterized thermophilic thiolase, these enzymes function as an in vitro synthetic pathway to produce acetone from acetyl-CoA at 70°C. The work reported here provides improved understanding of chemolithoautotrophic energy and carbon fixation pathways in the Sulfolobales, as well as thermostable enzymatic routes for production of 3HP and acetone. Together with rapidly improving molecular genetics techniques, these results constitute the first steps towards creation of a metabolically engineered Sulfolobus strain for production of volatile bio-based chemicals from inorganic carbon and energy sources. © Copyright 2018 by Benjamin Zeldes All Rights Reserved Leveraging Extreme Thermoacidophily for Archaeal Metabolic Engineering By Benjamin Zeldes A dissertation submitted to the Graduate Faculty of North Carolina State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Chemical Engineering Raleigh, North Carolina 2018 APPROVED BY: _______________________________ _______________________________ Dr. Robert M. Kelly Dr. Jason Haugh Committee Chair _______________________________ _______________________________ Dr. Rodolphe Barrangou Dr. Chase Beisel BIOGRAPHY Benjamin Monroe Zeldes was born in North Carolina to Steven Zeldes and Dru Monroe, but spent most of his childhood growing up in Arizona with his younger sister, Kristin. After high school, Ben attended the University of Pittsburgh, where he met his future wife Jennifer Huling. After graduating with degrees in Bioengineering (BS) and Political science (BA) in 2012, Ben decided to continue his education in the Department of Chemical and Biomolecular Engineering at North Carolina State University. Ben has spent the past several years studying a variety of exotic extremophiles under the advisement of Dr. Robert Kelly. After completing his PhD in June 2018, Ben plans to continue doing research with an eye towards an R&D career in biotechnology. ii ACKNOWLEDGMENTS I would like to thank my advisor, Dr. Robert Kelly, for his guidance and mentorship throughout graduate school. Whenever challenges come up during your PhD it is nice to hear from someone who has seen a quite a few of them and can give you some perspective. I would also like to thank past and present members of the Kelly lab, both for their emotional support and technical assistance throughout this process. Being surrounded by people who are passionate about research has made graduate school a rewarding and mostly fun experience. The NIH Molecular Biology Training program has provided excellent training, and afforded me opportunities to explore potential future career paths. Of course I would like to acknowledge my parents, for their loving support and encouragement throughout my life, and for inspiring me to be curious from an early age. My whole extended family has been supportive of my decision to pursue higher education. Many have graduate degrees themselves, and encouraged me to consider this path, either directly through conversations and advice, or simply by example. Finally, I would like to thank my wife, Dr. Huling, for her love and support, and for leading the way through this whole PhD process. iii TABLE OF CONTENTS LIST OF TABLES ..................................................................................................................... vii LIST OF FIGURES .................................................................................................................. viii CHAPTER 1 Extremely thermophilic microorganisms as metabolic engineering platforms for production of fuels and industrial chemicals .............................................. 1 1.1. Abstract ............................................................................................................................ 2 1.2. Introduction ...................................................................................................................... 3 1.3. Genetics in extreme thermophiles .................................................................................... 5 1.4. Candidates for high-temperature metabolic engineering ................................................. 8 Thermococcus kodakarensis ............................................................................................ 8 Pyrococcus furiosus ....................................................................................................... 10 Sulfolobus species .......................................................................................................... 14 Thermus thermophilus ................................................................................................... 17 1.5. Early stage genetic systems for extreme thermophiles .................................................. 18 Metallosphaera sedula:.................................................................................................. 18 Thermoanaerobacter mathranii: ................................................................................... 19 Caldicellulosiruptor bescii: ........................................................................................... 19 Thermotoga:................................................................................................................... 20 1.6. Overview of current state of industrial bioprocessing .................................................... 21 1.7. Future of extremely thermophilic metabolic engineering: challenges and promise ...... 22 1.8. References ...................................................................................................................... 38 CHAPTER 2 Ancillary contributions of heterologous biotin protein ligase and carbonic anhydrase for CO2 incorporation into
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