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Venomics of Sea Anemones: a Bioinformatic Approach to Tissue Specific Venom

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Venomics of Sea Anemones: A Bioinformatic Approach to Tissue Specific Venom Composition and Toxin Gene Family Evolution. DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Jason C. Macrander Graduate Program in Evolution, Ecology and Organismal Biology The Ohio State University 2016 Dissertation Committee: Dr. Marymegan Daly, Advisor Dr. John V. Freudenstein Dr. H. Lisle Gibbs Dr. Zakee L. Sabree Copyright by Jason C. Macrander 2016 Abstract Venom has independently evolved several times across diverse animal lineages, resulting in toxins targeting a variety of functionally important protein complexes and macromolecules involved in cellular homeostasis. Sea anemones (Actiniaria) are members of the oldest venomous animal lineage (Cnidaria) and use a diverse array of toxic peptides to incapacitate and immobilize prey, deter potential predators, and fight with conspecifics. When compared to other venomous lineages outside of Cnidaria, sea anemones are atypical venomous animals, as they have venom being expressed throughout their body, engage in conspecific aggression, and host ectosymbionts that are members of lineages that are typical food sources. For these reasons, sea anemones present an opportune lineage to ask questions about venom evolution in a comparative framework. For my dissertation, I use a combination of next-generation sequencing, bioinformatics, and gene tree reconstructions to a) characterize the toxin assemblage in an anatomical structure used exclusively in intraspecific aggressive encounters, b) contrast the toxin assemblage and differential gene expression across the tentacles, mesenterial filaments, and column in three species of sea anemones, c) investigate evolutionary processes and selection events shaping a neurotoxin gene family found exclusively in sea anemones, and d) characterize evolutionary history and functionally important regions in a pore forming toxin. In chapter 1, a tissue-specific RNA-seq approach is used to investigate the venom composition and gene ontology of acrorhagi, ii specialized structures used in intraspecific competition, in aggressive and non-aggressive polyps of the aggregating sea anemone Anthopleura elegantissima. The resulting assemblage of expressed genes may represent synergistic proteins associated with toxins or proteins related to the morphology and behavior exhibited by the aggressive polyp. In chapter 2, a tissue specific RNA-seq approach is used to characterize the venom assemblage in the tentacles, mesenterial filaments, and column for three species of sea anemone (Anemonia sulcata, Heteractis crispa, and Megalactis griffithsi). Across the different tissues and species, there was significant variation in abundance of toxin-like genes. In chapter 3, I use a broad taxonomic approach to characterize how sodium channel toxins (NaTxs) and type III potassium channel toxins (KTxs) have evolved across sea anemones. Toxin gene tree reconstruction and selection analyses show that type III KTx and NaTx genes sort into two distinct gene clusters with both venom types being taxonomically diverse. Overall, both toxin types are under negative selection, with some type III KTx gene clusters under positive selection and experiencing rapid diversification events. In chapter 4, a the evolutionary history of the pore forming toxins (actinoporins) is reconstructed to evaluate how this toxin type has evolved across sea anemones and how these toxins are related to actinoporin-like gene in sea anemones and other taxa. Additionally, I characterize variation in the functionally important residues across the actinoporin tree, supporting a recently proposed hypothesis for sphingomyelin recognition which differs significantly from what has been suggested traditionally. Overall, my dissertation contributes to the understanding of evolution, structure, and iii function in the ecologically and biomedically important toxin gene families found in sea anemones. iv Dedication This document is dedicated to my family. v Acknowledgments First I would like to thank my advisor Dr. Meg Daly for her guidance and encouragement throughout my Ph.D. I am also grateful to my committee members Dr. John Freudenstein, Dr. Lisle Gibbs, and Dr. Zakee Sabree for their continued guidance and support to my development as an independent scientist. Throughout my PhD I have also fostered collaborations and friendships with several wonderful scientists that have helped me along the way, including Dr. Mercer Brugler, Dr. Michael Broe, Joe Cora, Cheryl L. Ames, Dr. Estefania Rodriguez, Dr. Adam Reitzel, Annelise del Rio, Dr. Ray Norton, Michela Mitchell, Dr. Yehu Moran, Dr. Mande Holford, Dr. Paulyn Cartwright, Dr. Steven Sanders, and Sally Chang. I am also grateful for the pedagogical support through the Center for Life Science Education and University Center for the Advancement of Teaching at OSU and Dr. Joan Herbers for serving as a mentor with regards to diversity issues in STEM. I would like to thank all of my friends (too many to mention here) for their support and encouragement in addition to my wife Ashley Bowers-Macrander for her continued support and Amelia Macrander for showing me what is really important in life. My Ph.D. research was supported by the National Science Foundation (NSF), Columbus Zoo and Aquarium, the department of Evolution, Ecology, and Organismal Biology, and the National Evolutionary Synthesis Center. vi Vita 2002 ..............................................................Platteview High School 2007 ..............................................................B.S. Biology, University of Nebraska - Lincoln 2007 ..............................................................B.S. Fisheries & Wildlife, University of Nebraska - Lincoln 2010 ..............................................................M.S. Ecology, Evolution, and Behavior, University of Nebraska - Lincoln 2011 to present ............................................Graduate Teaching Associate/Graduate Research Associate, Department of Evolution, Ecology, and Organismal Biology, The Ohio State University Publications Mercier, A., Baillon, S., Daly, M., Macrander, J., Hamel, J.F. 2016. Biology of a deep- water sea anemone (Anthozoa: Actiniidae) from eastern Canada: spawning, development, and growth. Deep Sea Research Part II: Topical Studies in Oceanography, In Press Macrander, J. Broe, M, Daly, M. 2015. Multi-copy venom genes hidden in de novo transcriptome assemblies, a cautionary tale with the snakelocks sea anemone Anemonia sulcata (Pennant, 1977). Toxicon, 108: 184 – 188. vii Willis, S.C., Winemiller, K.O., Montaña, C.G., Reiss, P., Macrander, J., Farias, I.P., Orti, G. 2015. Population genetics of the speckled peacock bass (Cichla temensis), South America’s most important sport fishery. Conservation Genetics, 16: 1345 – 1357. Macrander, J., Brugler, M., Daly, M. 2015. A RNA-seq approach to identify putative toxins from acrorhagi in aggressive and non-aggressive Anthopleura elegantissima polyps. BMC Genomics, 16: 221. Nguyen, T., Collins-Silva, J., Podicheti, R., Macrander, J., Yang, W., Nazarenus, T., Nam, J., Jaworski, J., Lu, C., Scheffler, B., Mockaitis, K., Cahoon, E. 2012. Camelina seed transcriptome: A tool for meal and oil improvement and translational research. Plant Biotechnology Journal, 11: 759 – 69. Willis, S., Macrander, J., Farias, I., Orti. G. 2012. Simultaneous delimitation of species and quantification of interspecific hybridization in Amazonian peacock cichlids (genus Cichla) using multi-locus data. BMC Evolutionary Biology, 12: 96. Macrander, J., Willis, S.C., Gibson, S., Orti, G., Hrbek, T. 2012. Polymoprhic microsatellite loci for the Amazonian Peacock Basses, Cichla orinocensis and C. temensis, and cross-species amplification in other Cichla species. Molecular Ecology Resources doi: http://dx.doi.org/10.1111/j.1755-0998.2012.03173.x. Li C., Bessert, M. L., Macrander, J., Orti, G. 2009. Low variation but strong population structure in mitochondrial control region of plains topminnow, Fundulus sciadicus. Journal of Fish Biology, 74:1037 – 1048. Li C., Bessert, M. L., Macrander, J., Orti, G. 2007. Microsatellite loci for the plains topminnow (Fundulus sciadicus, Fundulidae). Molecular Ecology Notes, 7: 691 – 693. Fields of Study Major Field: Evolution, Ecology, and Organismal Biology viii Table of Contents Abstract ............................................................................................................................... ii Dedication ........................................................................................................................... v Acknowledgments.............................................................................................................. vi Vita .................................................................................................................................... vii List of Tables .................................................................................................................... xii List of Figures .................................................................................................................. xiv Chapter 1: A RNA-seq approach to identify putative toxins from acrorhagi in aggressive and non-aggressive Anthopleura elegantissima polyps. ..................................................... 1 Introduction ....................................................................................................................
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