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Molecular Investigation of the Cnidarian-Dinoflagellate Symbiosis

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Molecular Investigation of the Cnidarian-Dinoflagellate Symbiosis AN ABSTRACT OF THE DISSERTATION OF Laura Lynn Hauck for the degree of Doctor of Philosophy in Zoology presented on March 20, 2007. Title: Molecular Investigation of the Cnidarian-dinoflagellate Symbiosis and the Identification of Genes Differentially Expressed during Bleaching in the Coral Montipora capitata. Abstract approved: _________________________________________ Virginia M. Weis Cnidarians, such as anemones and corals, engage in an intracellular symbiosis with photosynthetic dinoflagellates. Corals form both the trophic and structural foundation of reef ecosystems. Despite their environmental importance, little is known about the molecular basis of this symbiosis. In this dissertation we explored the cnidarian- dinoflagellate symbiosis from two perspectives: 1) by examining the gene, CnidEF, which was thought to be induced during symbiosis, and 2) by profiling the gene expression patterns of a coral during the break down of symbiosis, which is called bleaching. The first chapter characterizes a novel EF-hand cDNA, CnidEF, from the anemone Anthopleura elegantissima. CnidEF was found to contain two EF-hand motifs. A combination of bioinformatic and molecular phylogenetic analyses were used to compare CnidEF to EF-hand proteins in other organisms. The closest homologues identified from these analyses were a luciferin binding protein involved in the bioluminescence of the anthozoan Renilla reniformis, and a sarcoplasmic calcium- binding protein involved in fluorescence of the annelid worm Nereis diversicolor. Northern blot analysis refuted link of the regulation of this gene to the symbiotic state. The second and third chapters of this dissertation are devoted to identifying those genes that are induced or repressed as a function of coral bleaching. In the first of these two studies we created a 2,304 feature custom DNA microarray platform from a cDNA subtracted library made from experimentally bleached Montipora capitata, which was then used for high-throughput screening of the subtracted library. In the second of these studies we used this array to profile the gene expression of bleached samples collected in Pilaa Bay, Kauai, HI. In both studies we detected a large number of host genes that displayed statistically different ratios of expression between the control and bleached groups of corals. The identified repressed genes included a novel carbohydrate associated protein (CnidCAP) putatively involved in host/symbiont specificity and recognition. Our data, particularly the emergence of CnidCAP, suggest that host/symbiont specificity in corals is homologous to the complement pathway active in innate immunity in animals. In addition, we have isolated many novel, unidentified genes that may prove useful as markers of coral stress. ©Copyright by Laura Lynn Hauck March 20, 2007 All Rights Reserved Molecular Investigation of the Cnidarian-dinoflagellate Symbiosis and the Identification of Genes Differentially Expressed during Bleaching in the Coral Montipora capitata by Laura Lynn Hauck A DISSERTATION submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Presented March 20, 2007 Commencement June 2007 Doctor of Philosophy dissertation of Laura Lynn Hauck presented on March 20, 2007. APPROVED: ____________________________________________ Major Professor, Representing Zoology ____________________________________________ Chair of the Department of Zoology ____________________________________________ 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. ____________________________________________ Laura Lynn Hauck, Author ACKNOWLEDGEMENTS The accomplishments of any individual are merely a reflection of that individual’s network of support. I have many people, professional and personal, to thank for helping me succeed in my graduate school experience. First I must give my advisor, Virginia Weis, a huge thank you. She has been a great advisor who has provided me with academic, intellectual and financial support while allowing me to grow as a scientist and ask the research questions that I truly wanted to ask. Virginia has also been a great role model, demonstrating that academia and family can coincide with one another. She overcame tremendous personal strife during the time that I was her student, with the loss of her spouse Mark Patterson, and she has handled it with a dignity and grace that is truly astounding. Thank you, Virginia, for being the inspiration that you are. I have been fortunate to have had a great graduate committee who guided my research and provided encouragement and enthusiasm along the way; my thanks to Kevin Ahern, Andy Karplus, Dahong Zhang, and Larry Curtis. I must also thank the many members of the Weis lab, former and present, for sharing their time, advise, expertise and friendship; many thanks to Wendy Phillips, Jodi Schwartz, Carys Mitchelmore, Melissa DeBoer, Maurico Rodriguez-Lanetty, Simon Dunn, Sophie Richier, Elisha Wood-Charlson and Christy Schnitzler. I must give particular thanks to Wendy Phillips, a true ‘lab goddess’, whose willingness to share her laboratory expertise was instrumental in the successful completion of my own laboratory work. On the same topic, I must also give Mauricio Rodriguez-Lanetty a special thank you for his guidance in the development, execution and analysis of my microarray experiments. Christy Schnitzler also patiently waded through stacks of baby paraphernalia, and suffered through diaper changes in our shared office and never once complained. I was also fortunate to have worked with two very talented undergraduate students, Morgan Packard and Marrisa Matzler, to whom I wish the best of luck in their future endeavors. My thanks must also go out to the folks at the Hawaii Institute of Marine Biology on Coconut Island, particularly Ruth Gates, Fenny Cox and Dave Krupp, for their assistance with my research activities there. On a personal note, “Yes Jeff, this does mean I am finally done with school!” I must thank my husband, Jeff Hauck, for being mostly tolerant of the fact that I have been in school the entire thirteen years (thus far) that we have been married. Seriously though, his support on my long scholastic journey is truly appreciated. I couldn’t have done this without you, Jeff, thanks! My parents, Nancy and John Lowas, taught me early on that I can do anything as long as I set my mind to it. Thanks for that lesson, and for all of the support and encouragement that you have provided to me throughout my life and in pursuit of this degree. It is nice to know that, no matter what, there are two people on this earth that absolutely believe in me. My daughter, McKenzie, has generously shared her mommy time, and made the whole journey worthwhile. I thank her for being a very good baby, allowing me to bring her to work with me every week until she was about 10 months old! That would not work well with the average baby; I was blessed with you. I would also like to thank my Grandma, Marjean Hatfield, for believing in my ability to finish what I started, and for giving me encouragement as I needed it. There are many friends that I need to thank as well. My undergraduate mentor, Sylvia Yamada, was my inspiration for continuing my education past the Bachelor’s degree. Sylvia, your friendship, mentoring, support and guidance has been truly appreciated, and was influential in shaping my entire scholastic career. Thank you so very much for everything. While I was able to bring McKenzie to work with me often, there are many research and teaching activities that are not conducive to the presence of a baby. My dear friend LaRae Wallace and I ‘care-swapped’ with our daughters making it possible for me to do a large portion of my research, all while Kira and McKenzie grew up together like sisters. Thanks! Finally, my Friday through Sunday sanity days with friends were key to my mental health throughout this process. I must thank Glen, Jeff & LeAnn, and Ron & Bonnie and for our many evenings of fun, and also thank Linda & Bob and Aimee’s Allstars for hours of softball entertainment. In addition, the motorcyclists of the ‘un-group’ patiently listened to my grumblings, tirades and triumph dialogs over beer at Friday Night Lodge, and joined me on the open road when I needed the escape from stress that can only be found on two wheels. Thanks to Sandy, Reid, Ted, Blinky, Randy, Rabbitt, Bill and the rest of the gang for waiting for me at the next road-stop. Cheers! CONTRIBUTION OF AUTHORS Wendy S. Phillips performed the Anthopleura elegantissima subtracted library from which CnidEF was isolated. She also sequenced the entire CnidEF cDNA prior to my analysis of the sequence. Steve J. Dollar is the contact for the Kauaii field site. He provided all background information on Pilaa Bay, and also arranged for access to this field site for sample collection. TABLE OF CONTENTS Page Chapter 1: General Introduction…………………………………………… 1 The Host ………………………………………………………..……….. 3 The Symbiont ………………………………………………….………... 6 The Symbiosis…………………………………………………………… 9 Breakdown of the Symbiosis……………………………………………. 14 The Adaptive Bleaching Hypothesis……………………………………. 16 Model Systems ………………………………………………………….. 17 Research Approach ……………………………………………………... 19 Thesis Chapters …………………………………………………………. 21 Chapter 2: Characterization of a novel EF-Hand homologue, CnidEF, in the
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