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Genetic and Biochemical Analysis of the Micrococcin Biosynthetic Pathway Philip Ross Bennallack Brigham Young University

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Genetic and Biochemical Analysis of the Micrococcin Biosynthetic Pathway Philip Ross Bennallack Brigham Young University Brigham Young University BYU ScholarsArchive All Theses and Dissertations 2016-11-01 Genetic and Biochemical Analysis of the Micrococcin Biosynthetic Pathway Philip Ross Bennallack Brigham Young University Follow this and additional works at: https://scholarsarchive.byu.edu/etd Part of the Microbiology Commons BYU ScholarsArchive Citation Bennallack, Philip Ross, "Genetic and Biochemical Analysis of the Micrococcin Biosynthetic Pathway" (2016). All Theses and Dissertations. 6182. https://scholarsarchive.byu.edu/etd/6182 This Dissertation is brought to you for free and open access by BYU ScholarsArchive. It has been accepted for inclusion in All Theses and Dissertations by an authorized administrator of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. Genetic and Biochemical Analysis of the Micrococcin Biosynthetic Pathway Philip Ross Bennallack A dissertation submitted to the faculty of Brigham Young University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Richard A. Robison, Co-Chair Joel S. Griffitts, Co-Chair Julianne H. Grose Steven M. Johnson Bradley C. Bundy Department of Microbiology and Molecular Biology Brigham Young University Copyright © 2016 Philip Ross Bennallack All Rights Reserved ABSTRACT Genetic and Biochemical Analysis of the Micrococcin Biosynthetic Pathway Philip Ross Bennallack Department of Microbiology and Molecular Biology, BYU Doctor of Philosophy Declining antibiotic discovery and flourishing antibiotic resistance have led to a modern antibiotic crisis which threatens to compromise our ability to treat infectious disease. Consequently, there is significant interest in developing new antibiotics with novel modes of action and chemical properties. Ribosomally synthesized and post- translationally modified peptides (RiPPs) are natural compounds with the appealing attributes of being derived directly from a genetic template while possessing numerous exotic chemical features that contribute to stability and antimicrobial activity. Abundant in nature, their diverse range of biological activities makes them excellent prospects for antibiotic development. Thiopeptides, a RiPP family rich in chemical complexity, represent a particularly promising example. Characterized by post-translationally formed sulfur- and nitrogen-containing heterocycles, more than 100 different thiopeptides have been identified from various cultivable bacterial producers, and the mining of genomic and metagenomic data promises to uncover many more chemical species that have eluded discovery by conventional means. These peptides are potent inhibitors of bacterial protein synthesis and have been shown effective against many drug-resistant pathogens. Despite these attractive properties, therapeutic applications have been limited by the lack of an efficient synthetic route and poor aqueous solubility. Both of these challenges would be greatly alleviated by a more complete understanding of thiopeptide biosynthesis and improved systems for analysis and engineering. Here we describe the characterization of a new thiopeptide gene cluster, which encodes the archetypal thiopeptide micrococcin P1. We describe the identification of the bioactive product and detail the mechanism of immunity in the producing strain. We also describe efforts to engineer this pathway for heterologous expression in Bacillus subtilis. Using this platform, we have been able to dissect this intricate biosynthetic pathway and parse the order and timing of the processing events involved in peptide maturation. The knowledge gained from these studies will inform future efforts to adapt thiopeptides for therapeutic use, and guide efforts to engineer unnatural compounds using the exotic enzymology employed by thiopeptide producing bacteria. Keywords: RiPPs, thiopeptides, micrococcin, peptide engineering, Bacillus subtilis ACKNOWLEDGEMENTS This work would not have been possible without the tremendous support of my two incredible advisors: Joel Griffitts and Richard Robison. Joel has been a phenomenal mentor, example and friend. His curious mind, enthusiasm for conquering the unknown and sense of humor has truly made this experience a joy and a thrill. Richard Robison has also been a fantastic mentor and tremendous source of encouragement. Rich has been one of the biggest champions of my successes, and I have appreciated the intellectual freedoms he has granted me whilst always making himself available for professional and personal advice. I feel truly honored to have been mentored by both of these great men but more importantly, to call them my friends. I also wish to acknowledge the many others who have contributed to this work. Members of my graduate committee — which also includes Steve Johnson, Julianne Grose and Brad Bundy — have provided invaluable insight and advice and been very influential in my academic development. Our collaborators at UCSF, Susan Miller and Kathryn Bewley have been amazing colleagues. Sue has provided a wealth of scientific insight and has been a true master of the literature. Kathryn has likewise been a great source of ideas and tremendous experimentalist. The assistance of these two remarkable scientists has been invaluable and has accelerated the pace and quality of my research. Many others in the department have contributed to my academic and personal development. From the multitude of undergraduate students who have assisted on this project to my fellow graduate students for their ideas and friendship, I express appreciation. To Kim O’Neill, Brad Berges, Don Breakwell, and other lunchroom companions I say “hello stupid!” Thanks for the laughs and friendly hallway greetings. These interactions have made this experience truly enjoyable and have made me feel at home in this department. I am eternally indebted to my parents for their unconditional support. My dear parents, Paul and Andrea Bennallack, have been my biggest advocates and have always supported all of my goals and decisions, even when they take me across the world. Ken and Carrie Perucca have treated me like their own son and have likewise supported our family in all aspects of life. With such wonderful people behind me, it has often felt impossible to fail. Finally, to my sweet girls Kaylee, Jayne and Elle, I dedicate this work. Kaylee has provided endless love, encouragement and (when needed) assistance at the bench. Never shy to embark on a new adventure, her faith in me and her optimism has provided clarity and motivation during good times and challenging times. Jayne and Elle, always so excited to visit Daddy at work, have helped me realize how blessed I am to work in such a friendly and intellectually stimulating environment. Knowing I have such a wonderful family to support is the best motivation to succeed. I will always cherish this incredible time in our lives. TABLE OF CONTENTS TITLE PAGE ................................................................................................................................... i ABSTRACT .................................................................................................................................... ii ACKNOWLEDGEMENTS ........................................................................................................... iii TABLE OF CONTENTS ................................................................................................................ v LIST OF TABLES .......................................................................................................................... x LIST OF FIGURES ....................................................................................................................... xi ABBREVIATIONS ..................................................................................................................... xiv Chapter 1. Introduction ................................................................................................................... 1 1.1 The need for new antibiotics ................................................................................................. 1 The antibiotic resistance crisis. ............................................................................................... 1 A brief history of antibiotics. .................................................................................................. 3 A return to antibiotic discovery. ............................................................................................. 4 Nature is the best chemist. ...................................................................................................... 5 Classes of natural products. .................................................................................................... 5 1.2 RiPPs: a new class of natural products ................................................................................. 8 Overview of RiPPs. ................................................................................................................. 8 Structure and classification. .................................................................................................... 9 Therapeutic potential. ........................................................................................................... 10 Peptide engineering and diversification. ............................................................................... 12 1.3 Thiopeptides: biosynthesis and engineering potential .......................................................
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