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Thermal Tolerance of Coral Photosymbionts: Genetic Factors and Strategies to Pursue Genetic Enhancement

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Thermal Tolerance of Coral Photosymbionts: Genetic Factors and Strategies to Pursue Genetic Enhancement Thermal tolerance of coral photosymbionts: genetic factors and strategies to pursue genetic enhancement Rachel A. Levin A thesis in fulfilment of the requirements for the degree of Doctor of Philosophy School of Biological, Earth, and Environmental Sciences Faculty of Science July 2017 THE UNIVERSITY OF NEW SOUTH WALES Thesis/Dissertation Sheet Surname or Family name: Levin First name: Rachel Other name/s: Ashley Abbreviation for degree as given in the University calendar: PhD School: Biological, Earth, and Environmental Sciences Faculty: Science Title: Thermal tolerance of coral photosymbionts: genetic factors and strategies to pursue genetic enhancement Abstract 350 words maximum: Dinoflagellates of the genus Symbiodinium form essential symbioses with reef building corals, underpinning the entire ecological foundation of coral reefs. Corals rely on photosynthate produced by Symbiodinium for their growth and calcification, which in turn forms the reef framework. Increased sea surface temperature due to climate change triggers the loss of Symbiodinium from corals (coral bleaching), which can result in coral death. Different genetic variants of Symbiodinium exhibit diverse thermal tolerances that influence the thermal bleaching thresholds of their coral host. However, despite decades of research into Symbiodinium biology, determinants of Symbiodinium thermal tolerance are still largely unresolved. Therefore, I aimed to unlock the basis of Symbiodinium thermal tolerance using a comparative physiology-genomics approach, and subsequently using this new knowledge, aimed to develop novel strategies that promote genetic manipulation of Symbiodinium. In this thesis, I discovered that thermal tolerance of type C1 Symbiodinium is driven by up-regulation of genes and functional gene groups responsible for sexual reproduction, scavenging of reactive oxygen species, and protein folding that maintain photosynthetic ability and limit reactive oxygen species production under heat stress. I also uncovered the first entire genome of a Symbiodinium virus along with hundreds of transcripts from viruses that infect Symbiodinium, whose transcriptional regulation under heat stress may contribute to Symbiodinium thermal sensitivity. Next, I successfully removed cell walls from live Symbiodinium to create the first Symbiodinium protoplasts and achieved Symbiodinium protoplast fusion, a key step in creating hybrid Symbiodinium cells with novel genetic combinations for ideal traits. Finally, using these discoveries, I developed a theoretical framework for Symbiodinium genetic engineering that incorporates Symbiodinium genetic elements, viral genetic elements, and Symbiodinium protoplasts, along with original genomic analyses of the potential for CRISPR/Cas9 gene editing in Symbiodinium. Together, the studies presented in this thesis unveil factors that govern, as well as strategies that may genetically enhance, Symbiodinium thermal tolerance. Declaration relating to disposition of project thesis/dissertation I hereby grant to the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or in part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all property rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstracts International (this is applicable to doctoral theses only). 10/07/2017 ……………………………………………………………………… ……………………………………………………………………… ……….………….. Signature Witness Signature Date The University recognises that there may be exceptional circumstances requiring restrictions on copying or conditions on use. Requests for restriction for a period of up to 2 years must be made in writing. Requests for a longer period of restriction may be considered in exceptional circumstances and require the approval of the Dean of Graduate Research. FOR OFFICE USE ONLY Date of completion of requirements for Award: i COPYRIGHT STATEMENT 'I hereby grant the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all proprietary rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstract International (this is applicableto doctoral theses only). I have either used no substantial portions of copyright material in my thesis or I have obtained permission to use copyright material; where permission has not been granted I have applied/will apply fora partial restriction of the digital copy of my thesis or dissertation.' Signed Date ......................... AUTHENTICITY STATEMENT 'I certify that the Library deposit digital copy is a direct equivalent of the final officially approved version of my thesis. No emendation of content has occurred and if there are any minor variations in formatting, they are the result of the conversion to dig�al format.' / Date ......... /P J/t.T....... ..................................... Originality statement I hereby declare that this submission is my own work, and to the best of my knowledge, it contains no materials previously published or written by another person or substantial proportions of material which have been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgement is made in the thesis. Any contribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project’s design and conception or in style, presentation and linguistic expression is acknowledged. Signed Date 10/07/2017 ii Publications during candidature Journal articles Levin RA, Beltran VH, Hill R, Kjelleberg S, McDougald D, Steinberg PD, van Oppen MJH (2016). Sex, scavengers, and chaperones: transcriptome secrets of divergent Symbiodinium thermal tolerances. Molecular Biology and Evolution 33: 2201-2215. Levin RA, Voolstra CR, Weynberg KD, van Oppen MJH (2017a). Evidence for a role of viruses in the thermal sensitivity of coral photosymbionts. The ISME Journal 11: 808-812. Levin RA, Suggett DJ, Nitschke MR, van Oppen MJH, Steinberg PD (2017b). Expanding the Symbiodinium (Dinophyceae, Suessiales) toolkit through protoplast technology. Journal of Eukaryotic Microbiology doi: 10.1111/jeu.12393. Levin RA, Suggett DJ, Voolstra, CR, Agrawal S, Steinberg PD, Suggett DJ, van Oppen MJH (2017c). Engineering strategies to decode and enhance the genomes of coral symbionts biology. Frontiers in Microbiology 8: 1220. Conference abstracts Levin RA, Hill R, van Oppen MJH, Steinberg PD, McDougald D (2014). From Symbiodinium heat stress to coral bleaching: a physiological timeline. Poster Presentation at the 15th International Symposium on Microbial Ecology. Gangnam-gu, Seoul, South Korea. Levin RA, Hill R, van Oppen MJH, Steinberg PD, McDougald D (2015). Comparative transcriptomics of Symbiodinium to identify genes that reduce coral bleaching. Poster Presentation at the 115th American Society for Microbiology General Meeting. New Orleans, Louisiana, United States of America. Levin RA, Beltran VH, Hill R, Steinberg PD, van Oppen MJH (2016). Symbiodinium exposed: transcriptomic basis of thermal tolerance. Oral Presentation at the 13th International Coral Reef Symposium. Honolulu, Hawaii, United States of America. iii List of main figures Chapter 2 Figure 1. Physiological detection of Symbiodinium heat stress .......................................... 13 Figure 2. Hierarchical clustering of DEGs ............................................................................ 16 Figure 3. Unsuccessful vs. successful acclimation to elevated temperature ...................... 21 Figure 4. Regulation of meiosis, ROS scavenging, and molecular chaperone genes .......... 26 Figure 5. Model of the molecular basis of Symbiodinium thermal tolerance and its impacts on Symbiodinium-coral symbiosis ...................................................................................... 30 Chapter 3 Figure 1. Genome of the novel +ssRNAV and its expression in Symbiodinium transcriptomes ................................................................................................................... 56 Figure 2. Viral infections and antiviral responses of Symbiodinium under heat stress ...... 59 Chapter 4 Figure 1. Cell wall digestion confirmed by cellulose staining and by swelling of protoplasts in hypotonic culture medium ............................................................................................. 91 Figure 2. Somatic hybridization (fusion) of Symbiodinium protoplasts .............................. 93 Figure 3. Single-cell photobiology throughout protoplast generation and cell wall regeneration ....................................................................................................................... 95 Figure 4. Physiological status of cultures
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