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Comparative Gene Analysis and Prediction of Innate Immunity and Apoptosis Machinery in Hydrothermal Vent Tubeworms Corey M

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Comparative Gene Analysis and Prediction of Innate Immunity and Apoptosis Machinery in Hydrothermal Vent Tubeworms Corey M University of Connecticut OpenCommons@UConn Master's Theses University of Connecticut Graduate School 8-22-2013 Comparative Gene Analysis and Prediction of Innate Immunity and Apoptosis Machinery in Hydrothermal Vent Tubeworms Corey M. Bunce University of Connecticut, [email protected] Recommended Citation Bunce, Corey M., "Comparative Gene Analysis and Prediction of Innate Immunity and Apoptosis Machinery in Hydrothermal Vent Tubeworms" (2013). Master's Theses. 497. https://opencommons.uconn.edu/gs_theses/497 This work is brought to you for free and open access by the University of Connecticut Graduate School at OpenCommons@UConn. It has been accepted for inclusion in Master's Theses by an authorized administrator of OpenCommons@UConn. For more information, please contact [email protected]. Comparative Gene Analysis and Prediction of Innate Immunity and Apoptosis Machinery in Hydrothermal Vent Tubeworms Corey M. Bunce B.S., University of Connecticut, 2009 A Thesis Submitted in the Partial Fulfillment of the Requirement for the Degree of Master of Science at the University of Connecticut 2013 i APPROVAL PAGE Master of Science Thesis Comparative Gene Analysis and Prediction of Innate Immunity and Apoptosis Machinery in Hydrothermal Vent Tubeworms Presented by Corey M. Bunce, B.S. Major Advisor: _____________________________________________ Spencer Nyholm Associate Advisor: _____________________________________________ Peter Girguis Associate Advisor: _____________________________________________ Adam Zweifach University of Connecticut 2013 ii Abstract Siboglinid tubeworms are an emerging model system for symbiosis in extreme conditions. At deep-sea hydrothermal vents in the Pacific Ocean, they harbor a chemoautotrophic symbiont in a specialized organ, the trophosome, where the bacteria carry out primary production via oxidation of reduced sulfur compounds. The trophosome of siboglinid worms is suggested to be tightly regulated, symbiont-responsive, and developmentally homeostatic. The purported mechanism involves a cellular proliferative or apoptotic response to bacterial signals, environmental cues, or nutrition. Though these processes are well understood in more amenable model systems, there has been little work uncovering the tubeworm’s genetic potential for sensing and responding to symbiotic stimuli by canonical means, including pattern recognition receptors, innate immune effectors, and apoptotic regulators. In the present work, bioinformatics methods are employed to identify homologs to known regulatory genes, within two siboglinid tubeworms, Ridgeia piscesae, and Riftia pachyptila. Homologs found in EST libraries from each worm are characterized and evaluated for functional relevance to symbiosis by protein prediction, domain matching, and phylogenetic reconstruction. The major protein families here observed are the peptidoglycan recognition proteins (PGRPs) and the Caspases, accompanied by an overview of the worm’s potential apoptotic suite of genes. The siboglinid set of potential PGRPs presents similar characteristics to non-hydrothermal vent-associated symbiotic organisms. As well, the siboglinid apoptosis network is neither enriched nor iii reduced for any core components. The caspase gene family includes two major groups, and overall resembles the structural assortment recently seen in most non-derived apoptosis networks, but may present properties unique among annelids. The results of these analyses provide a suite of potential symbiosis- related genes for future investigations. iv Acknowledgements I would first like to thank my major advisor, Dr. Spencer Nyholm, for the opportunity to do this work, and the guidance through it. As well, I thank all the members of the Nyholm Lab, past and present, for their insight, and harsh critiques. Our collaborators, Dr. Peter Girguis and his lab at Harvard have been indispensable in this process, and I thank them for all they’ve done making it possible. I’d also like to acknowledge the Joint Genome Institute (DOE) for their part in sequencing and analysis. I thank my family and friends for their support, continued interest, and for bearing with me. v Table of Contents Approval Page ii Abstract iii Acknowledgements v Table of Contents vi Main text 1 Chapter 1: Introduction 1 Chapter 2: General Methods 6 2.1: Animal Collection and Maintenance 6 2.2: EST Library Construction 6 2.3: Sequence Annotation and Analysis 7 2.4: Phylogenetic Reconstruction 7 2.5: End-Point PCR 8 2.5.1 RNA extraction and cDNA synthesis 8 2.5.2 PCR and Analysis 9 Chapter 3: Siboglinid Putative Pattern Recognition Receptors 9 3.1: Review of the Literature 9 3.2: Methodology 11 3.3: Results 11 Chapter 4: Apoptosis Pathway Comparison/Identification 16 4.1: Review of the Literature 16 4.1.1: Apoptosis in Siboglinid Tubeworms 16 4.1.2: Apoptosis Across Model Systems 18 4.2: Methodology 21 4.3: Results 23 Chapter 5: The Annelid Caspase Suite 26 5.1: Review of the Literature 26 4.2: Methodology 26 4.3: Results 27 Chapter 6: Discussion 29 Chapter 7: Conclusion 36 Appendices 39 vi Appendix I 39 Appendix II 40 Appendix III 41 References 42 vii Chapter 1: Introduction The physico-chemical characteristics of deep-sea hydrothermal vents are both extreme and erratic (Fisher et al. 2007; Nees et al. 2009; Moore et al. 2009). These spreading centers can be at depths over 2000m and have flow temperatures over 350°C, and even diffuse flow vents vary considerably in milieu composition over time. They also support highly productive ecosystems. Chemoautotrophic bacteria utilize reduced inorganic compounds in the vent fluid to drive carbon fixation. Just as nutritional symbioses are documented throughout familiar, stable, environments, the establishment of mutualistic relationships between these primary producers and multicellular eukaryotes has allowed for many invertebrate taxa, especially bivalves, crustaceans, and annelids, to dominate hydrothermal vent landscapes (Cavanaugh 1985; Dubilier et al. 2008). Though the fundamental nature of these nutritional symbioses are identical, hydrothermal vent chemosymbioses vary in symbiont phylotype, composition, and host morphology, and the faunal assemblages at vent sites can vary considerably in members and population sizes. In the Pacific Ocean, Siboglinid Annelid tubeworms are the prominent invertebrate taxa (Childress et al. 1987; Nees et al. 2009; Bright and Lallier 2010). Siboglinid species from hydrothermal vents host obligate binary relationships, each with a single species of Gammaproteobacteria. The adult worm lacks a mouth and gut, and derives all of its nutrion from the chemosymbiont, which resides in bacteriocytes within a specialized organ, the trophosome (Felbeck 1981; Cavanaugh 1985; Bright and Lallier 2010)(Fig. 1). 1 Figure 1 General anatomy of siboglinid tubeworms, including Ridgeia piscesae and Riftia pachyptila. Body plan shows the basis of the vascular system and branchial exchange with the environment. The trophosome does not come in contact with the external milieu. The two predominantly studied hydrothermal vent tubeworms are Riftia pachyptila and Ridgeia piscesae. Adult Riftia can grow over 2m in length with a tube diameter around 5cm, which can be over 100 times the size of an adult Ridgeia worm, but the major siboglinid anatomy does not vary. The tubeworm has a branchial plume, functionally similar to a gill, for metabolic exchange with the ambient water. This organ and the surrounding tissues constitute the worm’s direct contact with the environment. The vestimentum acts as an anchor, allowing the anterior plume to move up and down, and keeping the rest of the worm inside a chitinous tube. Each generation, the juvenile, which still contains a digestive system, settles on the vent substrate, and the bacterial symbiont invades through the body wall. Upon establishing the symbiosis, the worm’s digestive system degenerates, and it develops the trophosome, as well as the tube (Nussbaumer et al. 2006). To the best of our knowledge, the symbiont never again contacts the external environment during the life of the worm, and no 2 new symbiont invades the worm. The anatomical placement of the bacterial partner is the siboglinid’s major chemosymbiotic novelty. Other vent hosts maintain symbionts within gills, a gut, or superficially, reducing the distance required for metabolites to reach the chemoautotroph, and so decreasing the host’s exposure to the toxic vent chemicals (Dubilier et al. 2008; Childress and Girguis 2011). The tubeworm must pass all metabolites through its vasculature to the trophosome, where primary production takes place, and then move nutrients released by the indelible symbiont to the rest of the worm and export waste back through the plume into the environment (Bright and Lallier 2010; Childress and Girguis 2011). This arrangement can support some of the highest recorded carbon fixation and assimilation rates (Girguis and Childress 2006). Yet, analyses of these and other chemoautorophic symbioses suggests there is a substantial bacterial load which can be detrimental to the host when nutrients are limiting (Childress and Girguis 2011). The minimum bacterial population size required for rates of primary production suitable for host growth and maintenance may be far less than typically occupies the trophosome lobules when hydrogen sulfide, oxygen or other metabolites are abundant. Hydrothermal vents are believed to be unstable and potentially short lived. Research so far suggests Riftia displays different characteristics (metabolite
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