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ABSTRACT MCGUIRE, ASHLYN HENSON. When a Hemoglobin

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ABSTRACT MCGUIRE, ASHLYN HENSON. When a Hemoglobin ABSTRACT MCGUIRE, ASHLYN HENSON. When a Hemoglobin Acts as a Catalytic Enzyme: Mechanistic Studies of Dehaloperoxidase. (Under the direction of Dr. Reza A. Ghiladi). The marine hemoglobin dehaloperoxidase (DHP) from the terebellid polychaete Amphitrite ornata is the first multifunctional hemoprotein with both an O2-transport function and biologically- relevant peroxidase and peroxygenase activities. Previously, DHP was demonstrated to catalyze the oxidation of a wide variety of metabolites found in the environment A. ornata resides in, including halophenols, haloindoles, and pyrroles, as well as compounds of anthropogenic origin such as nitrophenols. Here, we will demonstrate the oxidation of another class of small-molecule pollutants, haloguaiacols, as well as nonnative substituted 4-R-guaiacols (R = NO2, MeO, Me), using dehaloperoxidase. Substrate oxidation and product identification were performed by utilizing biochemical assays monitored by both spectroscopic and spectrometric techniques. As representative substrates, 4-haloguaiacols (4-F-, 4-Cl-, and 4-Br-) undergo oxidative dehalogenation in the presence of DHP and hydrogen peroxide, yielding 2-methoxybenzoquinone (2-MeOBQ) as one of the primary products. 18O-labeling studies confirmed that oxygen incorporation was derived exclusively from water, consistent with substrate oxidation via DHP’s peroxidase activity. Stopped-flow UV-visible spectroscopic studies demonstrated that 2-MeOBQ was capable of reducing DHP from its peroxidase resting ferric oxidation state to the O2-transport active oxyferrous state, the latter of which was also determined to be capable of catalyzing guaiacol oxidation. Taken together, the results demonstrated here establish substituted guaiacols as a new class of DHP substrate that adds to an already diverse list, and further expands on the unique multifunctional nature of DHP and its ability to oxidize a wide range of toxic substrates, contributing to the survival of A. ornata. As DHP is a hemoenzyme, the reactivity of the previous substrates originates from the oxidation of Fe(III) protoporphyrin IX (PPIX) by H2O2 to Fe(IV). By replacing the heme with a structurally similar cofactor, changes in the enzymes reactivities were probed. The native heme cofactor is easily removed through Teale’s acid/butanone extraction; the apoenzyme could then uptake the new porphyrins (Mn-, Co-, Cu-PPIX and meso- and deutero-PIX). The reconstituted enzymes demonstrated both increased and decreased reactivity when compared. The metal- variants could not retain the native enzymes reactivity, but Fe-meso- and Fe-deutero-PIX demonstrated increased activities. Trihalophenol oxidation (peroxidase activity) turnover was increased 6-fold with the nonnative enzyme, while maintaining its catalytic efficiency. The oxidation of 1-methoxynaphthalene to Russig’s Blue (peroxygenase activity) demonstrated an increase in both the turnover number and the catalytic efficiency by 11-fold and 8-fold, respectively, for Meso-DHP. Mechanistic studies on the meso-PIX, deutero-PIX, and Mn-PPIX were also examined by stopped-flow UV-vis. New reactivities of DHP were also explored with both native DHP and the mutants. These processes included C-H activation chemistry: styrene epoxidations, sp3-hydroxlations, and carbene transfer chemistry. © Copyright 2020 by Ashlyn Henson McGuire All Rights Reserved When a Hemoglobin Acts as a Catalytic Enzyme: Mechanistic Studies of Dehaloperoxidase by Ashlyn Henson McGuire 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 Chemistry Raleigh, North Carolina 2020 APPROVED BY: _______________________________ _______________________________ Reza A. Ghiladi Stefan Franzen Committee Chair _______________________________ _______________________________ Elon Ison David Shultz BIOGRAPHY Ashlyn McGuire was born on October 19, 1992 to Lori and Randy Henson in Boone, North Carolina. She graduated high school from Watauga High. She attended Appalachian State University beginning in 2011 to study chemistry. During this time, she met her now husband, Wilson McGuire. After graduating with bachelor of science degree in Chemistry with Honors in 2015, she began graduate school in Chemistry at North Carolina State University and joined Dr. Reza Ghiladi’s research group. While attending North Carolina State University she was involved in several collaborations including a one-month travel fellowship in Spring 2017 to work with Dr. Pat Hutchings at the Australian Museum in Sydney to collect and analyze the hemoglobin of marine polychaetes. In Summer of 2017 and Spring of 2019, she travelled to Nagoya, Japan to work with Dr. Watanabe and Dr. Shoji of Nagoya University to study nonnative cofactor incorporation into dehaloperoxidase to expand the reactivity. She now lives in Durham, NC with her husband and pets, Arthur and Nala. ii ACKNOWLEDGMENTS I would like to express my gratitude to my family and friends who supported me during this stage of my life. Most especially, my husband, whose continued support and motivation was essential during the last five years. To my classmates and labmates (GG’s) who I’ve have been so lucky to meet and work alongside. I would also like to recognize my advisor, Dr. Reza Ghiladi for his guidance and continued support, both academic and personal, who afforded me the tools and opportunities to grow into a better scientist. iii TABLE OF CONTENTS LIST OF TABLES ........................................................................................................................ vi LIST OF FIGURES ..................................................................................................................... vii Chapter 1: Introduction .............................................................................................................. 1 1.1. Peroxidases ..................................................................................................................... 1 1.2. Peroxygenases ................................................................................................................. 2 1.3. Dehaloperoxidase ............................................................................................................ 2 1.4. Nonnative heme cofactors............................................................................................... 3 References ................................................................................................................................ 7 Chapter 2: Substituted Guaiacols as New Substrates for Dehaloperoxidase B from Amphitrite ornata: Mechanistic and Structural Studies ......................................................... 9 Abstract .................................................................................................................................... 9 Introduction ............................................................................................................................ 11 Experimental Procedures ....................................................................................................... 14 Results .................................................................................................................................... 18 Discussion .............................................................................................................................. 34 Conclusion ............................................................................................................................. 40 References .............................................................................................................................. 42 Supporting Information .......................................................................................................... 44 Chapter 3: Nonnative Heme Incorporation into Multi-functional Globin Increases Peroxygenase Activity an Order and Magnitude Compared to Native Enzyme ................. 59 Abstract .................................................................................................................................. 59 Introduction ............................................................................................................................ 61 Experimental Procedures ....................................................................................................... 63 Results .................................................................................................................................... 68 Discussion .............................................................................................................................. 88 Conclusion ............................................................................................................................. 91 References .............................................................................................................................. 93 Supporting Information .......................................................................................................... 96 Chapter 4: New Reactivies of Dehaloperoxidase: C-H Activation Chemistry ................... 121 Abstract ................................................................................................................................ 121 Introduction .......................................................................................................................... 122 Experimental
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