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Streptomyces Coelicolor: Genetic and Physiological Changes Induced by a Chemical Probe

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Streptomyces Coelicolor: Genetic and Physiological Changes Induced by a Chemical Probe The ARC2 Response in Streptomyces coelicolor: Genetic and Physiological Changes Induced by a Chemical Probe by Vanessa Yoon Calvelo A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Biochemistry University of Toronto © Copyright by Vanessa Yoon Calvelo 2021 The ARC2 Response in Streptomyces coelicolor: Genetic and Physiological Changes Induced by a Chemical Probe Vanessa Yoon Calvelo Doctor of Philosophy Department of Biochemistry University of Toronto 2021 Abstract Streptomyces are known for the production of biologically active secondary metabolites that are encoded in discrete gene clusters. Expression of these clusters is often controlled by factors that include growth rate, signaling molecules, metabolism, and physiological and environmental stresses. These diverse signals along with signal transduction proteins and transcription factors constitute a complex regulatory network that mediate various types of responses including the induction of secondary metabolism. In this work, I have taken a chemical genetic approach, using a chemical elicitor called ARC2, to investigate the regulatory network of Streptomyces coelicolor. I show that ARC2 alters the expression of primary metabolic genes associated with amino acid metabolism, carbohydrate metabolism, lipid metabolism and nucleic acid metabolism. I also show that ARC2 alters the expression of at least 16 different secondary metabolic gene clusters, including the gene cluster encoding the blue-pigmented secondary metabolite actinhorhodin. I go on to show that AfsR and AfsS, two regulators from the AfsK/AfsR/AfsS (AfsK/R/S) pleiotropic regulation system for secondary metabolism, are required for both the basal production of actinorhodin and the stimulation of actinorhodin production by the ARC2 elicitor. In addition, I show that the serine/threonine kinase AfsK is not required for actinorhodin production in S. coelicolor. Lastly, with the use of ARC2, I identified a functionally relevant repeat in the AfsS regulator that is required to activate secondary metabolism. This work demonstrates the use of a chemical tool to uncover novel aspects about the biology of secondary metabolism in the model organism S. coelicolor. ii Acknowledgments First, I would like to thank my supervisor Dr. Justin Nodwell for his patience and mentorship throughout my graduate studies. Thank you for taking a chance on me and welcoming me into your lab. With your guidance, I have grown tremendously as a scientist over the years and I hope to continue to grow in my next endeavour. I would also like to thank my past advisory committee members, Dr. Marie Elliot and Dr. Michael Surette, during my brief time at McMaster University as well as my current advisory committee members, Dr. Shana Kelley and Dr. Andrew Wilde, at the University of Toronto. Your feedback has always been appreciated. Second, I want to thank the past and present members of the Nodwell lab as you were the ones that provided a healthy and stable work environment. In particular, I want to thank Dr. Sheila Pimentel- Elardo and Dr. Stefanie Mak for the constant emotional and technical support both inside and outside of the lab. I also want to thank Saif Hossain for giving me the opportunity to gain mentorship experience, and I want to thank Jan Falguera for being just as excited about Streptomyces biology and committed to continuing this work. Lastly, a huge thank you to my family and friends for their encouragement and support. To my parents, thank you for all your hard work and sacrifices in supporting me throughout the course of my educational development. To my in-laws, thank you for always being kind and caring during this journey. To my husband Kevin Calvelo, thank you for your endless love and support in all aspects of our lives. Without all of you, I would not be where I am today. Finally, to my dogs Foster and Beauregard, thank you for being undeniably cute and the goodest of boys. *I would also like to acknowledge some of the life events that have made my Ph.D. experience that much more memorable: the passing of both my grandmothers, the passing of my family dog Toby, two physical lab moves, two flooding occurrences in my apartment, planning one wedding, two dead laptops, being asked and serving as a bridesmaid in six weddings, and one pandemic. iii Table of Contents Acknowledgments ........................................................................................................................ iii Table of Contents ......................................................................................................................... iv List of Tables ............................................................................................................................... vii List of Figures ............................................................................................................................. viii List of Appendices ........................................................................................................................ ix Chapter 1 Introduction ................................................................................................................ 1 Introduction ........................................................................................................................... 1 1.1 Streptomyces – a fascinating genus of bacteria ............................................................... 1 1.1.1 Features of Streptomyces genomes ............................................................................. 1 1.1.2 Multicellular development in Streptomyces ................................................................ 3 1.2 Secondary metabolism in Streptomyces .......................................................................... 9 1.2.1 Secondary metabolism in S. coelicolor ..................................................................... 12 1.2.2 Regulation of secondary metabolism in S. coelicolor .............................................. 19 1.3 Strategies to activate secondary metabolism ................................................................ 29 1.3.1 Genetic strategies ...................................................................................................... 30 1.3.2 Synthetic strategies ................................................................................................... 32 1.3.3 Ecological and chemical strategies ........................................................................... 34 1.4 Significance and Thesis Objectives .............................................................................. 38 Chapter 2 ARC2 remodels gene expression in S. coelicolor .................................................... 40 ARC2 remodels gene expression in S. coelicolor .............................................................. 41 2.1 Abstract ......................................................................................................................... 41 2.2 Introduction ................................................................................................................... 42 2.3 Results ........................................................................................................................... 44 2.3.1 ARC2 perturbs the S. coelicolor transcriptome ........................................................ 44 2.3.2 The effect of ARC2 on secondary metabolic genes .................................................. 71 2.3.3 The effect of ARC2 on primary metabolic genes ..................................................... 75 2.3.4 The effect of ARC2 on developmental genes ........................................................... 76 2.3.5 The effect of ARC2 on regulatory genes .................................................................. 78 2.4 Discussion ..................................................................................................................... 81 Chapter 3 afsK, afsR and afsS in the ARC2 response ............................................................. 85 afsK, afsR and afsS in the ARC2 response ........................................................................ 86 3.1 Abstract ......................................................................................................................... 86 3.2 Introduction ................................................................................................................... 87 3.3 Results ........................................................................................................................... 88 3.3.1 afsS and actII-ORF4 expression increases in response to ARC2 ............................. 88 3.3.2 afsR and afsS deletion, but not afsK deletion, compromises actinorhodin production 89 3.3.3 afsR and afsS deletion, but not afsK deletion, compromises the ARC2 response .... 91 3.4 Discussion ..................................................................................................................... 94 iv Chapter 4 A novel, functionally relevant repeat sequence in AfsS ........................................ 96 A novel, functionally relevant repeat sequence in AfsS ................................................... 97 4.1 Abstract ......................................................................................................................... 97 4.2 Introduction ................................................................................................................... 98
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