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AN ABSTRACT of the DISSERTATION of Damien E AN ABSTRACT OF THE DISSERTATION OF Damien E. Barrett for the degree of Doctor of Philosophy in Microbiology presented on September 17, 2020. Title: What Makes a Fish Resistant? Comparative Genomics and Transcriptomics of Oncorhynchus mykiss with Differential Resistance to the Parasite Ceratonova shasta Abstract approved: ______________________________________________________ Jerri L. Bartholomew The myxozoan Ceratonova shasta is an intestinal parasite of salmon and trout that causes ceratomyxosis, a disease characterized by severe inflammation of the intestine that can lead to hemorrhaging, necrosis, and death of the fish host. The parasite is endemic to the Pacific Northwest of the United States and Canada, where it has been linked to the decline of wild fish stocks. The parasite exerts a strong selective force on its fish host, and fish populations from C. shasta endemic watersheds become genetically fixed for resistance to ceratomyxosis. This contrasts with fish from watersheds where the parasite is not established, who are highly susceptible the disease, with a single spore capable of causing a lethal infection. Management of the disease relies on selective stocking of resistant fish, however, even these fish can succumb to the infection. Understanding the genetic and immunological basis of resistance to this disease would provide the framework for the development of therapeutics and identification of genetic markers that could be used in selective breeding. In this project, we employed a comparative transcriptomics and genomics approach to understand how resistant and susceptible strains of Oncorhynchus mykiss (rainbow trout/steelhead) respond to C. shasta infection and identify the genomic loci conferring resistance. We found that infection by C. shasta has an immunosuppressive effect in both resistant and susceptible fish, with IFNγ and interferon stimulated genes being downregulated in the gills, which is the portal of entry for the parasite. Once the parasite reaches the intestine, resistant fish quickly respond with an IFNγ driven TH1 response, and upregulation of MHC class I genes and genes involved in antigen processing and presentation. This response suggests that C. shasta has an intracellular phase during its migration to the intestine, which may represent a form of immune evasion that causes the host to initiate a cytotoxic T- cell response that is ineffective against the extracellular stages in the intestine. Susceptible fish, on the other hand, had no detectable immune response to the parasite reaching the intestine, highlighting the importance of parasite recognition in the different infection outcomes of these fish. In addition to a more rapid immune response, resistant fish have a tissue level response that limits the spread of the parasite within the intestine and allows them to regenerate their intestinal lining. Additionally, we have identified a region on chromosome Omy9 that significantly affects the odds of surviving C. shasta infection, and a region on Omy11 with a lesser contribution to survival. Taken together, this research represents a major step forward in our understanding of both the genetic and immunological basis of resistance to this important parasite. ©Copyright by Damien E. Barrett September 17, 2020 All Rights Reserved What Makes a Fish Resistant? Comparative Genomics and Transcriptomics of Oncorhynchus mykiss with Differential Resistance to the Parasite Ceratonova shasta by Damien E. Barrett A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented September 17, 2020 Commencement June 2021 Doctor of Philosophy dissertation of Damien E. Barrett presented on September 17, 2020. APPROVED: Major Professor, representing Microbiology Head of the Department of Microbiology Dean of the Graduate School I understand that my dissertation will become part of the permanent collection of Oregon State University libraries. My signature below authorizes release of my dissertation to any reader upon request. Damien E. Barrett, Author ACKNOWLEDGEMENTS It takes a village to raise a PhD, and for that I would like to sincerely thank everyone who has supported me through this process: My fellow graduate students; Laura Taggart-Murphy, Claire Howell, Kalyn Hubbard, and Benjamin Americus for assistance with fieldwork and for making the lab a warm and friendly place. Rich Holt for assistance with sampling and being a general wellspring of knowledge. Julie Alexander for maintaining the worm cultures that made these experiments possible. The staff at the Aquatic Animal Health Lab, in particular Ruth Milston-Clements and Ryan Craig for assisting with fish husbandry and for putting up with my many tank requests. Stephen Atkinson and Sascha Hallett for always being available to help and answer questions. The staff at the Center for Genome Research and Biocomputing, specifically Chris Sullivan, Shawn O’Neil, Matthew Peterson, and Andrew Black for their excellent instruction and Mark Desenko and Katie Carter for taking such good care of my samples. The Oregon Department of Fish and Wildlife, in particular William Tinniswood, and the staff at the Round Butte, Roaring River, and Alsea hatcheries for supplying the fish used in these studies. My graduate committee members; Dr. Michael Kent, Dr. Kelly Vining, Dr. Mike Blouin, and Dr. Kenneth Johnson for staying with me through a steep learning curve and providing valuable insights into my project. My advisor Dr. Jerri Bartholomew, for giving me the latitude to pursue such an ambitious project and for providing thoughtful critiques on my project and writing. And last but not least, my wonderful wife for supporting me through all of this and understanding the odd hours involved in this undertaking. CONTRIBUTION OF AUTHORS For the second manuscript, Dr. Itziar Estensoro processed tissue samples and interpreted the histology and Dr. Ariadna Sitjà-Bobadilla helped interpret the histology and provided valuable feedback on the manuscript. TABLE OF CONTENTS Page CHAPTER 1: INTRODUCTION ................................................................................................... 1 Introduction to myxozoa .......................................................................................................... 1 The myxozoan parasite Ceratonova shasta ............................................................................. 2 Factors affecting the outcome of infection ............................................................................... 2 Progression of the infection in the fish host ............................................................................. 4 Investigations into the mechanism of resistance ...................................................................... 5 Overview of the teleost immune system .................................................................................. 5 Studies on the antibody response to C. shasta ......................................................................... 6 Studies on the cytokine response during C. shasta infections ................................................. 7 The immune response in other fish-myxozoan systems........................................................... 9 Research objective.................................................................................................................. 13 REFERENCES .......................................................................................................................... 14 CHAPTER 2: A TALE OF TWO FISH: COMPARATIVE TRANSCRIPTOMICS OF RESISTANT AND SUSCEPTIBLE STEELHEAD FOLLOWING EXPOSURE TO CERATONOVA SHASTA HIGHLIGHTS DIFFERENCES IN PARASITE RECOGNITION .... 24 ABSTRACT .............................................................................................................................. 25 INTRODUCTION ..................................................................................................................... 25 TABLE OF CONTENTS (Continued) Page MATERIAL AND METHODS................................................................................................. 29 Fish ......................................................................................................................................... 29 Parasite challenge ................................................................................................................... 29 Sample collection ................................................................................................................... 30 Sample processing .................................................................................................................. 31 Sequencing ............................................................................................................................. 31 Data analysis .......................................................................................................................... 32 RNA-seq validation by quantitative reverse transcription PCR (RT-qPCR) ......................... 33 RESULTS .................................................................................................................................. 33 Infection of resistant and susceptible fish stocks ................................................................... 33 qPCR quantification of parasite burden ................................................................................. 36 Sequencing ............................................................................................................................
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