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Horizontal Gene Transfer in the Sponge Amphimedon Queenslandica

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Horizontal Gene Transfer in the Sponge Amphimedon Queenslandica Horizontal gene transfer in the sponge Amphimedon queenslandica Simone Summer Higgie BEnvSc (Honours) A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2018 School of Biological Sciences Abstract Horizontal gene transfer (HGT) is the nonsexual transfer of genetic sequence across species boundaries. Historically, HGT has been assumed largely irrelevant to animal evolution, though widely recognised as an important evolutionary force in bacteria. From the recent boom in whole genome sequencing, many cases have emerged strongly supporting the occurrence of HGT in a wide range of animals. However, the extent, nature and mechanisms of HGT in animals remain poorly understood. Here, I explore these uncertainties using 576 HGTs previously reported in the genome of the demosponge Amphimedon queenslandica. The HGTs derive from bacterial, plant and fungal sources, contain a broad range of domain types, and many are differentially expressed throughout development. Some domains are highly enriched; phylogenetic analyses of the two largest groups, the Aspzincin_M35 and the PNP_UDP_1 domain groups, suggest that each results from one or few transfer events followed by post-transfer duplication. Their differential expression through development, and the conservation of domains and duplicates, together suggest that many of the HGT-derived genes are functioning in A. queenslandica. The largest group consists of aspzincins, a metallopeptidase found in bacteria and fungi, but not typically in animals. I detected aspzincins in representatives of all four of the sponge classes, suggesting that the original sponge aspzincin was transferred after sponges diverged from their last common ancestor with the Eumetazoa, but before the contemporary sponge classes emerged. In A. queenslandica, the aspzincins may have been co-opted for multiple functions, since 54 of the 90 fit into one of four ontogenetic expression profiles, each of which is putatively co-expressed with different suites of native genes. Based on secretion signals and the conservation of key catalytic residues, I propose that proteolytic activity is maintained in at least one of the aspzincin roles in A. queenslandica. Mobile elements are capable of genomic excision, movement and integration, they enable HGT in bacteria, and some animal HGTs are genomically close to eukaryotic transposable elements (TEs); as such, mobile elements are speculated as possible players in the mechanisms of interkingdom and interdomain HGT to animals. In A. queenslandica, the overall repeats densities around predicted unduplicated HGTs are not different to those around predicted unduplicated native genes. However, ii the surrounding repeats content of unduplicated HGTs has slightly increased proportions of the helitron DNA transposon and of simple repeats. Further, 29% of the HGT-derivatives are TEs, half of which are unknown in class, a quarter are copia long terminal repeats retrotransposons and the other quarter are helitrons. These data suggest that repeats and TEs may have putative roles in the HGT process in animals, such as simple repeats possibly conferring increased chances of genomic integration through recombination and helitrons perhaps increasing chances of HGT functionality via their reservoir of regulatory elements. Another seven per cent of the HGT-derivatives have high sequence similarities to proteins present on bacterial plasmids, suggestive that plasmids were involved in some of the transfers. Together, these results offer novel insight on HGT in A. queenslandica and demonstrate that HGT has a varied nature in this animal with an extensive impact, partially due to post-transfer duplications. Further, this work offers insights on possible mechanisms that led to the HGT derived genes of this sponge. iii Declaration by author This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, financial support and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my higher degree by research candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis and have sought permission from co-authors for any jointly authored works included in the thesis. iv Publications during candidature Conference Abstracts Higgie, S. S. and S. M. Degnan, 2016. Trans-domain horizontal gene transfer from bacterium to animal: the post-transfer evolution of the aspzincins in the sponge Amphimedon queenslandica. Society for Molecular Biology and Evolution (SMBE), Gold Coast, QLD, Australia, 3-7 July 2016. Publications included in this thesis No publications included. v Contributions by others to the thesis Sandie M. Degnan contributed to the conception and design of this research, advised on methods and analysis, and provided critical comments on the thesis. Selene L. Fernandez-Valverde produced several of the datasets analysed in this thesis (as specifically acknowledged in the relevant chapters). William L. Hatleberg produced the genome-wide BLAST2Go and Pfam annotations for Aqu2.1 gene models, as specifically acknowledged in Chapter 3. William L. Hatleberg also modified a published script that was used to test for Pfam domain enrichments (as specifically acknowledged in Chapter 3). Federico Gaiti developed the script used in Chapter 3 for the co-expression analysis (as specifically acknowledged in Chapter 3). Statement of parts of the thesis submitted to qualify for the award of another degree None. Research involving human or animal subjects No animal or human participants were involved in this research. vi Acknowledgements For the last seven years, I have been a member of the Degnan Laboratories in a few roles, so it is with great warmth (and disbelief!) that I write these acknowledgements. First, to my advisor Sandie Degnan. Thank you for sharing your expertise and for all your help, guidance, and enthusiasm during my project. You have given me a lot of patience, freedom, and time to find my way and I appreciate that. I have always respected your seemingly endless supply of curiosity and passion for science and feel privileged to have you as a role model in both science and life, thank you for your continued support. Thank you to my co-advisor Sassan Asgari, I appreciate your time and comments. I am also very appreciative to my readers Mark Ragan and Matt Sweet for always being at important milestones throughout my project, for their critique, suggestions, and encouragement. In addition, thank you to my committee chair Jan Engelstädter for his time and for providing valuable feedback. I am grateful to the Australian Government for an Australian Postgraduate Award and thus the financial opportunity to undertake this quest for greater understanding. I also appreciate a travel award from the School of Biological Sciences, which enabled me to attend the Society for Molecular Biology and Evolution (SMBE) 2016 conference. Thanks also to Gail Walter, the efficient and patient postgraduate administrator for the School of Biological Sciences. To both joint lab Heads, Sandie and Bernie Degnan, thank you for developing my research questions, skills and career over the last seven years. I am grateful for the world-class research facilities, environment and opportunities you have given me, including two weeks in the field on the beautiful Heron Island of the Great Barrier Reef and a trip to Japan to attend the 12th ISDCI congress. Related, a huge thanks to all past and present Deglabsters for your large part in making the lab a vibrant and diverse community, both scientifically and socially. Laura, Federico, Andrew, Carmel, William, Tahsha, Kerry, Selene, Jabin, Kevin, Bec, Ben, Aude, Maely, Katia, Daniel, Shun, Jo, Felipe, Jaret, Nobuo, Gemma, Nick, Markus, vii Claire, Mel, Yasu, Emily, Arun, Eunice, Xueyan, Romy, and Lisa – your comradeship, assistance and advice with all things science, computers, and life in general are much appreciated. More specifically, I am hugely grateful to Selene Fernandez-Valverde for her invaluable help with the mysterious “black screen”, that is, for her bioinformatics and programming expertise and help! Special thanks also to Sandie and Selene for our collaborative HGTracker project, the results of which formed the starting point
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