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Applications of Resonance Raman Spectroscopy to the Study of Bioinorganic Macromolecules

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Applications of resonance Raman spectroscopy to the study of bioinorganic macromolecules DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Pearson T. Maugeri, B.S. Biophysics Graduate Program The Ohio State University 2017 Dissertation Committee: Professor Hannah S. Shafaat, Advisor Professor James A. Cowan Professor Terry L. Gustafson Professor Marcos Sotomayor © Copyright by Pearson T. Maugeri 2017 Abstract Transition metals are absolutely critical for the existence and maintenance of biologi- cal systems. Many cellular processes, such as metabolism, the detoxifying of harmful chemicals, gene regulation, and extracellular signaling rely on the unique properties that metal cofactors provide. One very important group of metalloproteins is the ferritin-like superfamily. The ferritin-like superfamily contains proteins that have a large array of functions, ranging from the storage and transport of essential nutri- ents such as iron and oxygen (ferritin and hemerythrin) to the 2-electron oxidation of the stable C-H bonds found in hydrocarbons (di-iron hydroxylases). Of particular interest are the ribonucleotide reductases, enzymes that catalyze the de novo syn- thesis of deoxyribonucleotides from ribonucleotides. Additionally, different classes of ribonucleotide reductases use dissimilar sets of metals to achieve similar end results. In 2009, a novel protein group called the R2-like ligand-binding oxidases, or R2lox, was discovered. The function of R2lox is not currently known, although it does do 2-electron chemistry, as seen by a novel Tyr-Val linkage that forms during the acti- vation of oxygen. This new class of proteins exhibits sequence similarity to the R2 subunit of the ribonucleotide reductases and is reminiscent of bacterial multicom- ponent monooxygenses (BMMs) in both the bound ligand and also its hypothesized chemistry. It has been shown that this protein is upregulated in the virulent strain of Mycobacterium tuberculosis, and therefore it is of great interest to uncover the role that this protein plays in its various hosts. ii There are many ways to study bioinorganic systems; however, one of the most ver- satile and sensitive techniques is spectroscopy. Many different wavelength regimes are able to be plied to furthering the understanding of bioinorganic systems. One of the most useful types of spectroscopy in a chemist’s toolbox is vibrational spectroscopy, due to the opportunity that it affords to extract structural information. One typeof vibrational spectroscopy is Raman scattering, which uses inelastically scattered pho- tons to report on the vibrational modes of a molecule. Furthermore, the resonance Raman phenomenon can and has been used to great effect in bioinorganic systems by tuning the Raman excitation beam to an electronic absorption, enhancing the signal and making resonance Raman spectroscopy a very useful tool for the study of bioinorganic structure and function. This thesis presents two main projects that are different in character. The first is the development of a custom variable wavelength resonance Raman experimental sys- tem. A brief background of resonance Raman scattering is presented before outlining the layout of the experimental setup. Collaborations with other research groups were also conducted, and the custom resonance Raman system was used to probe a wide range of bioinorganic systems. The other section of the thesis details experiments on R2lox. One chapter outlines the investigation of an unusual phenomenon where the optical properties of R2lox change drastically upon irradiation with light. The other chapter discusses setting up R2lox to be probed via transient absorption so that electron transfer constants may be extracted. iii For Charlene, my dearest love iv Acknowledgments No man is an island, Entire of itself, Every man is a piece of the continent, A part of the main. The above excerpt from John Donne’s 1623 work, Meditations XVII: Devotions upon Emergent Occasions, is an absolutely spot on summary of what my academic experience has been up to this point. I could not have done any of this without the firm and unyielding support that I have received from friends, family and fellow academics. I am truly not an island. First, I would like to acknowledge my advisor, Dr. Hannah Shafaat. She has provided an excellent model of scientific excellence to emulate. I would like to thank her for giving me the opportunity to work in her group and to assemble the custom resonance Raman system, which is detailed in chapter 3. I would also like to thank Dr. Dongping Zhong, in whose lab I gained a lot of my fundamental understanding of ultrafast laser systems as well as biological spectroscopy. In addition, thank you to my thesis committee, who sacrificed their time to give me good feedback on this document as well as on my research projects. Each of you have helped me grow as a scientist and I am very grateful for your mentorship. I would also like to thank my collaborators on the projects discussed in this work. Thank you to Dr. Cowan, Dr. Jingwei Li, and Stephen Pearson for collaborating with me on the project in chapter 6. To Dr. Thomas Rauchfuss and Michaela Carlson, v thank you for your collaboration on the project described in chapter 7. Thank you to Dr. Kyle Lancaster, Dr. John Caranto, and Avery Vilbert for the collaboration on the project described in chapter 8. Special thanks to Dr. Martin Högbom, Dr. Julia Griese, and Dr. Rui Branca for all of your help in running experiments in the study described in chapter 4, including providing mutants, as well as all of your helpful discussions regarding R2lox. Thank you to all for your contributions to this work. I would also like to thank my labmates in the Shafaat research group. Each and every one of you has affected my academic life for the better and I would not be here if it wasn’t for your influence. Thank you Tasha, for helping me to integrate intothis lab and for providing me with someone to bounce ideas off and for watching my dog on the rare occasions I got out of town. Thank you Jeff for all the discussions about Game of Thrones, and for all your help with the resonance Raman system. Thank you Cami for all your help with troubleshooting the labeling conditions in Chapter 5 and for our discussions on the pros and cons of OSU football. Thank you Shelby for helping me with my inorganic chemistry knowledge, especially with point groups, and for all our geeky conversations about video games. I would also like to thank Dr. Michael Stevenson, who provided me with an invaluable viewpoint of the academic process though the lens of a postdoctoral researcher. We will always have Akron. Thank you Sean for being a good TA partner when we taught CHEM 4310. You made teaching that class much more enjoyable. Thank you Effie for your help in all of the R2lox purification and experiments as well as for being a good officemate the past year despite my, shall we say, less than orderly desk. I will look back on all of our discussions about how finicky R2lox is with fondness. I have been blessed beyond measure to have been afforded the opportunity to work and grow scientifically with all of you during my time here. I would also like to thank my undergraduate professors at Harding University vi who nurtured my love for science. Thank you Dr. Stewart for teaching me how to think outside of the box and solve puzzles in organic synthesis. I have applied that skill to so many other things here at OSU. Thank you Dr. Matlock for taking time out of your day to speak with me about biochemistry and to help me transition to thinking in a more biophysical context. Finally, I would like to thank Dr. Murray, who was so patient with me when I was fumbling around in his upper-level physics courses and had no idea what I was doing. Thank you all for showing me that one can simultaneously be a scientist and a man of God. Finally, I would like to extend my boundless appreciation to family, who has listened to my joys and my frustrations for these last several years. They have always been a source of unwavering support and I cannot thank them enough for everything they have done. Finally, thank you to my amazing wife, Charlene. I would not have finished if it wasn’t for you. You have been by my side this whole time andIamso thankful that were always ready to listen when I had bad news and celebrate with me when I had good news. I would like to thank each and every person who has helped me in my academic journey, but there is not enough room in this document for that. Again, I am in no way an island and the work described herein, while it has my name on it, would simply not have been possible without a massive amount of assistance and support from an incalculable number of sources. vii Vita February 17, 1990 . Born, Gainesville, FL May 2008 . Dacula High School, Dacula, GA May 2012 . B.S. in Biochemistry and Molecular Bi- ology, Harding University, Searcy, AR September 2012 to August 2014 . Graduate Teaching Associate, Depart- ment of Chemistry and Biochemistry and Department of Physics, The Ohio State University September 2014 to August 2015 . CMBP Fellow, Cellular, Molecular, and Biochemical Sciences Training Pro- gram, The Ohio State University September 2015 to present . Graduate Teaching Associate, Depart- ment of Chemistry and Biochemistry Publications Slater, J. W., Marguet, S. C., Cirino, S. L., Maugeri, P. T. & Shafaat, H. S. Ex- perimental and DFT Investigations Reveal the Influence of the Outer Coordination Sphere on the Vibrational Spectra of Nickel-Substituted Rubredoxin, a Model Hydro- genase Enzyme.
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