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Analysis of Secreted Enzymes, Metabolism and Virulence in the Bat Fungal Pathogen Pseudogymnoascus Destructans

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Analysis of Secreted Enzymes, Metabolism and Virulence in the Bat Fungal Pathogen Pseudogymnoascus destructans By Chapman N. Beekman B.A., Wheaton College (MA), 2010 Thesis Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Division of Biology of Medicine at Brown University PROVIDENCE, RHODE ISLAND May, 2019 © Copyright 2019 Chapman N. Beekman This dissertation by Chapman N. Beekman is accepted in its present form by the Department of Molecular Biology, Cell Biology and Biochemistry as satisfying the dissertation requirement for the degree of Doctor of Philosophy. Date_________________ ________________________________ Dr. Richard J. Bennett, Advisor Recommended to the Graduate Council Date_________________ ________________________________ Dr. Mark Johnson, Reader Date_________________ ________________________________ Dr. Alison DeLong, Reader Date_________________ ________________________________ Dr. Peter Belenky, Reader Date_________________ ________________________________ Dr. Robert A. Cramer, Jr, Reader Approved by the Graduate Council Date_________________ ________________________________ Dr. Andrew Campbell, Dean of the Graduate School iii Acknowledgements I would not have gotten to this point without the help of many people along the way. Firstly, I would like to thank my advisor Richard Bennett for pushing me to be the best scientist I can be while also allowing me the freedom to pursue my scientific curiosities throughout my PhD. Your guidance, advice and support has been instrumental throughout this project. I would also like to thank my committee members: Alison DeLong, Mark Johnson and Peter Belenky for your advice and perspective throughout our meetings and discussions and for your genuine interest in seeing me succeed. I would also like to thank my former mentors, especially Robert Obar from whom I learned an incredible amount during my time as a research assistant. I am also extremely grateful to Anthony O’Donoghue and Giselle Knudsen, whom have served as collaborators, friends, and mentors during this time. They brought not only their expertise but also a level of energy and positivity that has inspired and motivated me throughout my PhD. I am especially grateful for the time they took to train and mentor me during my visit to their labs. A special thanks goes to Gigi for showing me around San Francisco, Mission street and introducing me to the best burrito I have ever had in my life. Thank you also to the MCB graduate program, Mark, Judith, Elaine, Ashley and Ray as well as the MMI department, Cheny, Sam, Denise and Michelle for all of your work which makes mine and other’s research at Brown possible. I would also like to thank the members of the Bennett lab both past and present as well as others in MMI and MCB who have been great friends and colleagues. Jules Ene especially, who has been a great friend and second mentor throughout my time in lab. I would also like to thank my mentee Eleanor Kim for her work and contribution to this project. I would also like to thank all my friends who have been a constant source of support and entertainment. I truly feel blessed to have all of you in my life and I sincerely doubt I would have made it through the challenges of graduate school without you. A special thanks to my best man Jeff, our wedding officiants Ben and Nick, and Amy whom have been there for me and Currie since the first year of college at Wheaton, as well as Andy and Lyvia who have always kept a spot for us to crash when visiting Boston …or now Maine. I would also like to thank skateboarding, which as my second (or first) passion has provided me with a physical and creative outlet throughout my PhD and through which I have met many awesome people including Luke and Mason whom have been great friends since elementary school. I would also like to thank my family for their love and unwavering support throughout my life. My Parents especially, who have always supported me in whatever goal I set forth and have always been willing to listen and help in any way possible with whatever challenges or decisions I am facing. You are also the hardest working people I know and you have been a source of inspiration for me throughout my PhD and my life. Lastly, I would like to thank my wife Currie. Currie, you have been my best friend and partner throughout grad school and well before, and you have helped keep me sane during the most challenging times. You are the first person I come to whether I have good news or bad. You have always been there for me and made me feel incredibly loved like the several times you have stayed with me in the lab until 3 or 4 in the morning just to keep me company while I try and finish an experiment. I wouldn’t have been able to get to this point without you, so thank you! iv Table of Contents Signature Page…………………………………………………………………………………..iii Acknowledgements……………………………………………………………………………...iv Table of Contents………………………………………………………………………………...v List of Figures and Tables………………………………………………………………………ix CHAPTER 1: INTRODUCTION ....................................................................................... 1 The threat of emerging fungal pathogens .................................................................... 2 Saprophytic growth and its connection to pathogenicity .............................................. 3 Chytridiomycosis: a recent example of the destructive capability of invasive fungi ...... 4 Pathogenesis of chytridiomycosis and Snake Fungal disease: devastating cutaneous infections .................................................................................................................... 5 Secreted proteins and virulence in mammalian fungal pathogens ............................... 7 Secreted peptidases in mammalian fungal pathogens ...............................................11 The emergence and impact of White-nose Syndrome in bats ....................................16 The Pathology of WNS...............................................................................................17 The role of host immune responses during WNS .......................................................18 Differences in host susceptibility to WNS: resistance vs. tolerance ............................20 Origins of P. destructans and WNS: An invasive fungal pathogen .............................22 Morphology, growth and niche-range of P. destructans..............................................23 Phylogenic history of P. destructans and cross-species comparisons ........................24 Putative virulence factors in P. destructans ................................................................26 Existing tools to study virulence in P. destructans (this will be quick) .........................27 Overview ....................................................................................................................27 Figures .......................................................................................................................29 References ................................................................................................................32 CHAPTER 2: Characterization of PdCP1, a Serine Carboxypeptidase from Pseudogymnoascus destructans, the Causal Agent of White-nose Syndrome ..... 46 Abstract .....................................................................................................................48 Introduction ................................................................................................................49 Results .......................................................................................................................52 v Secretome analysis in P. destructans and related species .....................................52 Recombinant expression and purification of PdCP1 ...............................................53 Analysis of PdCP1 substrate specificity ..................................................................55 Characterization of PdCP1 activity using AMC substrates ......................................56 Discussion .................................................................................................................58 Materials and Methods ...............................................................................................63 Strains and culture media .......................................................................................63 Secretome generation ............................................................................................63 Generation of recombinant PdCP1 expression constructs ......................................64 Transformation of P. pastoris ..................................................................................64 PdCP1 expression and purification .........................................................................65 SDS-PAGE .............................................................................................................66 Fluorescent peptidase assays ................................................................................66 MSP-MS assay .......................................................................................................67 Mass Spectrometry ................................................................................................67 Acknowledgements ....................................................................................................70 Figures .......................................................................................................................71
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