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Venomics of Sea Anemones: A Bioinformatic Approach to Tissue Specific Venom Composition and Toxin Gene Family Evolution.

Macrander, Jason C

Abstract Details

2016, Doctor of Philosophy, Ohio State University, Evolution, Ecology and Organismal Biology.
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, 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 function in the ecologically and biomedically important toxin gene families found in sea anemones.
Marymegan Daly (Advisor)
John Freudenstein (Committee Member)
Lisle Gibbs (Committee Member)
Zakee Sabree (Committee Member)
231 p.

Recommended Citations

Citations

  • Macrander, J. C. (2016). Venomics of Sea Anemones: A Bioinformatic Approach to Tissue Specific Venom Composition and Toxin Gene Family Evolution. [Doctoral dissertation, Ohio State University]. OhioLINK Electronic Theses and Dissertations Center. http://rave.ohiolink.edu/etdc/view?acc_num=osu1461063376

    APA Style (7th edition)

  • Macrander, Jason. Venomics of Sea Anemones: A Bioinformatic Approach to Tissue Specific Venom Composition and Toxin Gene Family Evolution. 2016. Ohio State University, Doctoral dissertation. OhioLINK Electronic Theses and Dissertations Center, http://rave.ohiolink.edu/etdc/view?acc_num=osu1461063376.

    MLA Style (8th edition)

  • Macrander, Jason. "Venomics of Sea Anemones: A Bioinformatic Approach to Tissue Specific Venom Composition and Toxin Gene Family Evolution." Doctoral dissertation, Ohio State University, 2016. http://rave.ohiolink.edu/etdc/view?acc_num=osu1461063376

    Chicago Manual of Style (17th edition)