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    Role of the P-cluster and FeMo-cofactors in nitrogenase catalysis
    (Montana State University - Bozeman, College of Letters & Science, 2017) Keable, Stephen Michael Keable; Chairperson, Graduate Committee: John W. Peters; Andrew J. Rasmussen, Karamatullah Danyal, Brian J. Eilers, Gregory A. Prussia, Axl X. LeVan, Lance C. Seefeldt and John W. Peters were co-authors of the article, 'Three structural states of the nitrogenase P-cluster revealed in MOFE protein structures at poised potentials' submitted to the journal 'Biochemistry' which is contained within this thesis.; Jacopo Vertemara, Karamatullah Danyal, Andrew J. Rasmussen, Brian J. Eilers, Oleg A. Zadvornyy, Luca De Gioia, Giuseppe Zampella, Lance C. Seefeldt and John W. Peters were co-authors of the article, 'Acetylene interaction with the nitrogenase femo-cofactor investigated by structural and computational analysis' submitted to the journal 'Biochemistry' which is contained within this thesis.; Dissertation contains two articles of which Stephen Michael Keable is not the main author.
    Biological nitrogen fixation has been extensively researched for over four decades, yet due to the complex nature of this process, numerous questions still remain regarding the catalytic mechanism, and investigation of this system has relevance across a number of disciplines. Nitrogen is a fundamental element to all biological systems, primarily occurring in proteins and nucleic acids. However, most nitrogen on Earth is found in the form of nitrogen gas, a form that is biologically unavailable to most organisms owing to the strength of the triple bond between the two nitrogen atoms. The limited abundance of biologically accessible (or fixed) nitrogen has driven an anthropomorphic thrust to supplement the nitrogen cycle with nitrogenous fertilizers, thereby boosting agricultural output. The primary industrial method to produce these fertilizers, derived from the Haber-Bosch synthesis, is an energy intensive process that consumes approximately 1- 2% of the world's energy portfolio. This process utilizes metal iron catalysis, high temperatures and high pressures, along with hydrogen usually obtained from reformed fossil fuels, to reduce atmospheric nitrogen gas to ammonia. Aside from the environmental consequences that arise from the production of nitrogenous fertilizers, long-term agricultural application may also have disastrous ecological ramifications, such as eutrophication. Additionally, biological nitrogen fixation supports more than half the human population, and having a more complete understanding of this complex process has the potential to displace some of the demand for fertilizer production. The aforementioned reasons are clearly enough to warrant serious investigation into biological nitrogen fixation, however, the fascinating intricacies and comparative relevance to other biochemical systems further motivates the study of this system. The enzyme committed to this task, nitrogenase, orchestrates an elegant unidirectional multiple electron reduction and activation of the nitrogen triple bond. Historically, mechanistic characterization of this enzyme has been difficult for a number of reasons; however, studies to date have revealed many aspects of the process as biochemical techniques have improved. Nitrogenase is an oxygen sensitive, complex two-component enzyme that is mechanistically pertinent to many other biochemical processes. Presented here are studies revealing insight into substrate binding and the unique gated electron transfer mechanism of this fascinating enzyme.
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    Nucleotide dependent conformational changes in the nitrogenase Fe protein
    (Montana State University - Bozeman, College of Letters & Science, 2005) Sen, Sanchayita; Chairperson, Graduate Committee: John W. Peters
    Nitrogenase is a complex metal-containing enzyme that catalyzes the conversion of nitrogen gas to ammonia. During nitrogenase catalysis the Fe protein and the molybdenum-iron protein associate and dissociate in a manner resulting in the hydrolysis of two molecules of MgATP and the transfer of at least one electron to the MoFe protein. The role of nucleotide binding and hydrolysis in nitrogenase catalysis is one of the most fascinating aspects of nitrogenase function. The Fe protein upon binding to MgATP undergoes a huge conformational change which is important for subsequent steps of nitrogenase reaction mechanism. Therefore structural characterization of the Fe protein bound to MgATP will provide a basis on how MgATP binding promotes the complex formation whereas hydrolysis to MgADP leads to the dissociation of the macromolecular complex structure. Towards these ends we have conducted structural studies on a site-directed variant of the Fe protein which is a close mimic of the MgATP conformational state. Structural characterization of this Leu127 deletion variant revealed a distinctly new conformation of the Fe protein which arises from the rigid body reorientation of the homodimeric Fe protein subunits with respect to each other. The structure not only provides the first basis on rationalizing the initial docking interactions between the component proteins but also helps us to dissect the conformational changes on the Fe protein which occur upon nucleotide binding from those conformational changes that are imposed on the Fe protein by the MoFe protein during complex formation. Having this structure in hand, we have developed several other experimental approaches like Mass spectrophotometry and Small Angle X-ray Scattering/Diffraction (SAXS) techniques to probe the relationship between the Leu127 deletion variant a close structural mimic of MgATP bound "on state" and the actual MgATP bound state which is more difficult to probe crystallographically. These studies will help us to compare the different nucleotide bound states (MgADP and MgATP) of the Fe protein in solution that will help to predict the level of conformational change that is induced in the Fe protein that makes it compatible for binding to the MoFe protein in the nitrogen catalysis cycle.
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    Defining the ecological interactions that drove the evolution of biological nitrogen fixation
    (Montana State University - Bozeman, College of Letters & Science, 2012) Hamilton, Trinity Lynn; Chairperson, Graduate Committee: John W. Peters; Eric S. Boyd and John W. Peters were co-authors of the article, 'Environmental constraints underpin the distribution and phylogenetic diversity of NIFH in the Yellowstone geothermal complex' in the journal 'Microbial ecology' which is contained within this thesis.; Rachel K. Lange, Eric S. Boyd and John W. Peters were co-authors of the article, 'Biological nitrogen fixation in acidic high-temperature geothermal springs in Yellowstone National Park, Wyoming' in the journal 'Environmental microbiology' which is contained within this thesis.; Marcus Ludwig, Ray Dixon, Eric S. Boyd, Patricia C. Dos Santos, Joao C. Setubal, Donald A. Bryant, Dennis R. Dean and John W. Peters were co-authors of the article, 'Transcriptional profiling of nitrogen fixation in Azotobacter vinelandii' in the journal 'Journal of bacteriology' which is contained within this thesis.; Marty Jacobson, Marcus Ludwig, Eric S. Boyd, Donald A. Bryant, Dennis R. Dean and John W. Peters were co-authors of the article, 'Differential accumulation of NIF structural gene MRNA in Azotobacter vinelandii' in the journal 'Journal of bacteriology' which is contained within this thesis.
    All life requires fixed forms of nitrogen (N). On early Earth, fixed N was supplied through abiotic mechanisms, which became limiting to an expanding biome, precipitating the emergence of biological nitrogen fixation. Today, most biological nitrogen fixation is catalyzed by molybdenum (Mo)-dependent nitrogenase (Nif). Alternative forms of the enzyme contain either vanadium (V) or only iron (Fe) instead of Mo, but are only found in taxa that encode Nif. Geochemical evidence suggests Mo bioavailability was limited on the early Earth, leading to the hypothesis that alternative forms of nitrogenase are ancestral. Evidence presented here suggests that in fact Nif emerged first in a methanogenic archaeon. Previous studies revealed a widespread distribution of nif along geochemical gradients but little is known about the environmental conditions that drove its evolution. An analytical approach allowed examination of the role environment played in shaping the evolution of Nif across geochemical gradients in Yellowstone National Park. The distribution of nifH was widespread and not constrained by temperature or pH alone, but exhibited evidence of niche conservatism imposed by salinity, and seemed dispersal limited. Activity measurements in sediments collected from high-temperature acidic springs confirmed the potential for N ₂ fixation in these environments. These data expand our understanding of the habitat range and environmental drivers of N ₂ fixing organisms. In organisms that encode alternative nitrogenases, Nif is preferred for nitrogen fixation. In addition, the alternative forms of the enzyme do not encode the full suite enzymes necessary for assembling the active site metal cofactors. Presumably, the selective pressure driving the evolution of alternative nitrogenase would have been provided by Mo limitation. Transcriptome studies of a model organism which encodes all three forms of nitrogenase reveals the genes associated with expression of each nitrogenase and the interplay between systems that enables nitrogen fixation in the absence of Mo and fixed N. These analyses suggest the alternative nitrogenases would not function in the absence of Nif biosynthetic machinery and expression of nitrogenase is regulated by fixed N limitation and metal availability. The results presented here help elucidate the environmental conditions that have driven nitrogenase evolution, resulting in the extant enzyme.
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