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Chloe Van Der Burg Thesis UNDERSTANDING THE ROLE OF INNATE IMMUNE AND NOVEL GENES IN THE EVOLUTION AND REGENERATION OF SEA ANEMONES Chloé Annelies van der Burg Bachelor of Applied Science Bachelor of Biomedical Sciences (Honours) Submitted in fulfilment of the requirements for the degree of DOCTOR OF PHILOSOPHY School of Biomedical Science Faculty of Health Queensland University of Technology 2020 Keywords Actiniaria, bioinformatics, Cnidaria, comparative, de novo, differential gene expression, evolution, Exaiptasia pallida, gene expression, gene ontology, genome, immunome, innate immune system, lineage-specific, NACHT domain, next- generation sequencing, novel genes, phylogenetic, regeneration, RNAseq, sea anemones, selection, sequencing, taxonomically-restricted, timecourse, TIR domain, transcriptome Understanding the role of innate immune and novel genes in the evolution and regeneration of sea anemones i Abstract Phylum Cnidaria (sea anemones, hydroids, coral and jellyfish) is a metazoan lineage and the sister phylum to Bilateria. Understanding the evolution of genes within cnidarian lineages can provide insights into key conserved metazoan traits, while also elucidating how taxon-specific processes can evolve or become restricted to certain lineages. In this thesis I investigate three major aims, which broadly seek to provide insight into the evolutionary relationship between the innate immune system and regeneration in actiniarians (sea anemones), and place this in the context of other cnidarian and invertebrate species. To achieve this, I have generated multiple genomic and molecular data sets and performed multiple lines of bioinformatic, phylogenetic and evolutionary analyses. This includes but is not limited to: generating transcriptomic resources for multiple previously uncharacterised sea anemones, generating a fully replicated RNAseq time course experiment, performing differential expression analysis, inferring phylogenetic relationships and selective pressures acting on actiniarian genes. This thesis shows that actiniarians maintain a suite of core metazoan innate immune genes that are highly conserved and that the dominant selection pressure on innate immune genes is purifying, with some instances of episodic diversifying selection. I observe several novel, sea anemone-specific innate immune genes and novel architectures within conserved innate immune genes. This suggests possible compensatory mechanisms within Actiniaria that drives innovation in the innate immune system. I also observe maintenance of a more ancestral composition in conserved protein family domains within innate immune gene families, with episodic and diversifying selection primarily reflecting species-level evolutionary patterns. Together, this suggests classical immune gene architectures evolved in an early sea anemone or cnidarian ancestor, and that local gene family evolution and expansion is likely related to the diverse environmental niches of different sea anemone species. Here, in line with the general consensus in the literature, I provide evidence that the expression of the innate immune system is restricted to early time points during regeneration in the actiniarian species Exaiptasia pallida. I observe regeneration in E. pallida to be very rapid and shows a high level of tissue plasticity, driven by an early ii Understanding the role of innate immune and novel genes in the evolution and regeneration of sea anemones transcriptional burst of genes related to cell communication, signalling and remodelling. I identify a suite of uncharacterised species-specific genes as well as conserved genes in E. pallida that appear to work in concert to achieve regeneration. I also observe that the majority of genes recruited during E. pallida regeneration are unique to actiniarians, however, this taxonomic restriction is observed primarily due to gene loss in other taxa, as the majority of these genes evolved before Cnidaria split from Bilateria. Overall, I provide insights into the conservation, expansion, diversification and unique selective pressures acting on the actiniarian gene repertoire, and provide insights into how taxonomically restricted processes may evolve and utilise both conserved and novel gene systems. Understanding the role of innate immune and novel genes in the evolution and regeneration of sea anemones iii A Note Regarding Format This thesis is presented as a thesis by monograph. However, sections of this thesis have been published as research articles. For this reason, a “Statement of Contribution of Co-Authors for Thesis by Published Paper” is included at the beginning of relevant chapters. Chapter two “Insights into the innate immunome of actiniarians using a comparative genomic approach” has been published as a research article in BMC Genomics. The details of this publication are provided at the beginning of Chapter two. The chapter has been presented as-is in the publication, with minor formatting changes to be cohesive with the thesis structure. Chapter three “The rapid regenerative response of a model sea anemone species Exaiptasia pallida is characterised by tissue plasticity and highly coordinated cell communication” has been published as a research article in Marine Biotechnology. For the purpose of the thesis structure, some sections in the publication have been presented in Chapter four, and a small section of work that is included in Chapter three is not included in the publication. Details of the publication can be found at the beginning of Chapter three. Lastly, the sea anemone species Exaiptasia pallida was only recently named as such and was previously known primarily as Aiptasia pallida, although several entries for different Aiptasia species (including A. californica, A. diaphana, A. insignis and A. pulchella) have now been consolidated as this one species (Grajales & E. Rodríguez, 2016). In one chapter (Chapter 2) in this thesis the species is referred to as Aiptasia pallida, as this is how the species was described in the published manuscript and so this has not been changed in this chapter in order to remain consistent with the publication. In addition to this, the first genome assembly is officially recorded as the ‘Aiptasia genome v1.0’ (Baumgarten et al., 2015), and many publications cited herein refer to this species as Aiptasia, so in some instances it is appropriate to refer to the species as such. iv Understanding the role of innate immune and novel genes in the evolution and regeneration of sea anemones Table of Contents Keywords ...................................................................................................................... i Abstract ........................................................................................................................ ii A Note Regarding Format ........................................................................................... iv Table of Contents ......................................................................................................... v List of Figures ........................................................................................................... viii List of Tables................................................................................................................ x List of Supplementary Figures ...................................................................................... xi List of Supplementary Tables .................................................................................... xii List of Abbreviations................................................................................................. xiv List of Publications .................................................................................................... xv Statement of Original Authorship ............................................................................ xvii Acknowledgements ................................................................................................. xviii Chapter 1: Introduction ...................................................................................... 1 1.1 Tissue repair and regeneration ............................................................................ 1 1.2 Orphan genes, lineage-specific genes and novel gene networks ........................ 4 1.2.1 Horizontal gene transfer (HGT) ................................................................ 6 1.3 Regeneration and the immune system ................................................................ 7 1.4 Mechanisms and modes of regeneration in Cnidaria .......................................... 9 1.5 Exaiptasia pallida as a model for regeneration ................................................. 12 1.6 Conclusion ........................................................................................................ 13 1.7 Research plan .................................................................................................... 15 1.7.1 Aim 1/Study 1 ......................................................................................... 15 1.7.2 Aim 2/Study 2 ......................................................................................... 15 1.7.3 Aim 3/Study 3 ......................................................................................... 16 Chapter 2: Insights into the innate immunome of actiniarians using a comparative genomic approach .............................................................................. 17 Abstract .....................................................................................................................
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