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Onset and Breakdown of Cnidarian-Dinoflagellate Symbiosis

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Onset and Breakdown of Cnidarian-Dinoflagellate Symbiosis AN ABSTRACT OF THE DISSERTATION OF Sheila A. Kitchen for the degree of Doctor of Philosophy in Zoology presented on January 29, 2016. Title: Onset and Breakdown of Cnidarian-Dinoflagellate Symbiosis: A Survey of the Host Transcriptomic Response and Characterization of the Sphingosine Rheostat during Symbiont Colonization and Hyperthermal Stress Abstract approved: ______________________________________________________ Virginia M. Weis The symbiosis between cnidarians, such as corals and sea anemones, and photosynthetic dinoflagellates belonging to the genus Symbiodinium spp. is one of the most productive in the marine environment. This mutualistic endosymbiosis allow reef- building corals to lay down the foundation of coral reef ecosystems, which supports a highly biodiverse community of marine organisms. The relationship between the cnidarian host and algal symbiont changes over time, from the initial contact through symbiont removal. The breakdown of the partnership can be brought on by numerous environmental stressors; most notably by elevated temperatures associated with climate change. The cellular and molecular mechanisms underlying these key events in cnidarian- dinoflagellate symbiosis are still poorly understood. Lipids play a central role in symbiosis by providing cellular structure, energy storage, signaling platforms. Specifically, the signaling lipids from the sphingosine rheostat, sphingosine and sphingosine-1-phosphate (S1P), play a pivotal role in determining cell fate. Increased sphingosine drives apoptotic activity within the cell while S1P promotes cell survival. The research presented in this dissertation addresses (1) the role of signaling sphingolipids at different stages of cnidarian-dinoflagellate symbiosis and (2) the transcriptional patterns of coral larvae undergoing onset of symbiosis while exposed to elevated seawater temperatures. In Chapter 2, the proposed cnidarian sphingosine rheostat model was functionally characterized in the sea anemone Aiptasia pallida. This study identified differential response of the sphingosine rheostat with symbiont recolonization and long-term symbiont maintenance, suggesting a role in host-symbiont interactions. In Chapter 3, a heat stress experiment revealed a biphasic sphingosine rheostat response in A. pallida where acute stress inhibits rheostat expression and activity that is recovered and shifted toward cell death with longer-term heat stress. This response was not linked to symbiont loss, but has implications for a more generalized heat stress response for long-term acclimation in cnidarians. In Chapter 4, coral Acropora digitifera larvae displayed different phenotypes and transcriptional profiles with the combined stress of elevated temperature and symbiont uptake. Larval survival, symbiont colonization and algal density were highly reduced from this treatment. These transcriptional patterns indicate immune suppression, membrane reorganization and oxidative stress. Furthermore, sphingolipid signaling differed at the onset of heat stress. Overall, the work presented here indicates that the sphingosine rheostat mediates host- symbiont interactions until symbiosis dysfunction and that the determinants of symbiosis can be altered with climate-induced stress. ©Copyright by Sheila A. Kitchen January 29, 2016 All Rights Reserved Onset and Breakdown of Cnidarian-Dinoflagellate Symbiosis: A Survey of the Host Transcriptomic Response and Characterization of the Sphingosine Rheostat during Symbiont Colonization and Hyperthermal Stress by Sheila A. Kitchen A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented January 29, 2016 Commencement June 2016 Doctor of Philosophy dissertation of Sheila A. Kitchen presented on January 29, 2016 APPROVED: Major Professor, representing Zoology Chair of the Department of Integrative Biology 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. Sheila A. Kitchen, Author ACKNOWLEDGEMENTS I would like to express sincere appreciation for the encouragement and support of my advisor, Dr. Virginia Weis. Over the course of my time in the Weis Lab, she continued to “fill my glass” with her optimism and insights. She has made significant strides to improve my scientific communication and deepen my understanding of symbiosis. Furthermore, she provided many opportunities for me to explore my interests leading to a collaboration with researchers in Japan that allowed me to do field work, developing curriculum for invertebrate biology and symbiosis classes and engaging in non- dissertation projects. I would like to thank my committee members Drs. Jerri Bartholemew, Dee Denver, John Fowler, and Barb Taylor for their feedback and technical assistance throughout my time at OSU. Additionally, I would like to specially thank Drs. Eli Meyer, Chuya Shinzato and Duo Jiang for their significant contributions to my scientific training. Both Eli and Chuya generously allowed me to work in their lab spaces and were instrumental to my bioinformatic training that allowed me to analyze the high-throughput sequencing data in this dissertation and other various collaborative projects. Duo played an important role in building my confidence with statistical analyses of small and big datasets and our conversations contributed greatly to the analyses in Chapter 4. A special thanks to the Weis Lab members, past and present, that have created a collaborative and productive working environment. From the lab, I would like to recognize Angela Poole, Cammie Crowder, Trevor Tivey and Nate Kirk, all of whom have kept me sane throughout graduate school and research woes. Angela not only made significant contributions to my transition in the lab with training on all things Aiptasia and our various collaborative projects, but she has been the most supportive and thoughtful friend outside of the lab. I would like to thank Cammie, Trevor and Nate for allowing me to bother them with scientific and often non-scientific questions. In addition, I would like to thank a couple undergraduates that contributed to my research projects: Jessica Flesher helped with the experimental design and execution of Aiptasia bleaching ACKNOWLEDGEMENTS (Continued) in Chapter 3 and Jamie Jo McGraw contributed to the Symbiodinium RNA extraction protocol in Chapter 2. Finally, I want to show my appreciation for the continued support from my friends and family during this long process. Their reassurance and optimism in my abilities to succeed did not go unnoticed. I cannot thank them enough for providing happy distractions when I was overwhelmed. CONTRIBUTION OF AUTHORS Dr. Angela Z. Poole assisted in the experimental design, collection and analysis of the symbiotic state and colonization qPCR data from Chapter 2. Dr. Poole also significantly contributed to preparation of the Appendix. Dr. Duo Jiang provided feedback on the statistical approaches used to analyze symbiont colonization, algal density and gene expression data in Chapter 4. Moreover, she performed the analysis of the survival data. Dr. Saki Harii assisted in both designing and performing the 2013 and 2014 larval colonization experiment. She performed pilot studies in 2013 on temperature tolerance of A. digitifera larvae, facilities for rearing adult colonies and larvae, and Symbiodinium cultures. Dr. Noriyuki Satoh provided laboratory equipment, reagents and financial support for high-throughput sequencing at Okinawa Institute of Science and Technology. Dr. Chuya Shinzato contributed significantly to the design, execution and analysis of the larval colonization experiment in Chapter 4. He assisted in the collection of samples, preparation of sequencing libraries, and provided resources from the A. digitifera genome necessary to perform RNASeq. Dr. Virginia M. Weis contributed significantly to the experimental design of each chapter. She provided equipment, reagents and space to complete Chapters 2 and 3, and computational resources to analyze the data from Chapter 4. In addition, her feedback was influential in the development and writing of each chapter. TABLE OF CONTENTS Page 1. Introduction ..................................................................................................................... 1 1.1 Initiation and establishment of cnidarian-dinoflagellate symbiosis .......................... 1 1.2 Breakdown of cnidarian-dinoflagellate symbiosis in a changing world ................... 3 1.3 Lipids are regulators of symbiosis ............................................................................. 5 1.4 A. pallida and A. digitifera: Two model systems used to investigate cnidarian- dinoflagellate symbiosis .................................................................................................. 7 1.5 References ............................................................................................................... 11 2. Sphingolipids in cnidarian-dinoflagellate interactions: investigating the role of the sphingosine rheostat during onset of symbiosis and at steady-state in Aiptasia pallida .. 19 2.1 Summary .................................................................................................................. 20 2.2 Introduction ............................................................................................................
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