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Investigating Diversity, Evolution, Development and Physiology of Red Algal Parasites from New Zealand

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Investigating Diversity, Evolution, Development and Physiology of Red Algal Parasites from New Zealand Investigating diversity, evolution, development and physiology of red algal parasites from New Zealand BY MAREN PREUSS A thesis submitted to Victoria University of Wellington in fulfilment of the requirements for the degree of Doctor of Philosophy Victoria University of Wellington Te Whare Wānanga o te Ūpoko o te Ika a Māui (2018) ii This thesis was conducted under the supervision of Associate Professor Joe Zuccarello (Primary Supervisor) Victoria University of Wellington, Wellington, New Zealand and Professor Wendy Nelson (Secondary Supervisor) National Institute of Atmospheric Research, Wellington, New Zealand and University of Auckland, Auckland, New Zealand iii iv Abstract Red algal parasites have evolved independently over a 100 times and grow only on other red algal hosts. Most parasites are closely related to their host based on the similarity of their reproductive structures. Secondary pit connections between red algal parasites and their hosts are used to transfer parasite organelles and nuclei into host cells. Morphological and physiological changes in infected host cells have been observed in some species. Parasite mitochondrial genomes are similar in size and gene content to free-living red algae whereas parasite plastids are highly reduced. Overall, red algal parasites are poorly studied and thus the aim of this study was to increase the general knowledge of parasitic taxa with respect to their diversity, evolutionary origin, development, physiology, and organelle evolution. Investigation of the primary literature showed that most species descriptions of red algal parasites were poor and did not meet the criteria for defining a parasitic relationship. This literature study also revealed a lack of knowledge of many key parasitic processes including early parasite development, host cell “control”, and parasite origin. Many of these poorly studied research areas were addressed in this thesis. Phylogenetic analyses, using a range of markers from all three genomes (cpDNA: rbcL, nDNA: actin, LSU rRNA; mtDNA: cox1), showed different patterns of phylogenetic relationships for the four new red algal parasites and their hosts. The parasites Phycodrys novae-zelandiophila sp. nov. and Vertebrata aterrimophila sp. nov. closest relative is its host species. Cladhymenia oblongifoliophila sp. nov. closest relative is its host species based on nuclear and mitochondrial markers whereas the plastid markers group the parasite with Cladhymenia lyallii, suggesting that the parasite plastid was acquired when previously parasitizing C. lyallii. Judithia parasitica sp. nov. grows on two Blastophyllis species but the parasites’ closest relative is the non-host species Judithia delicatissima. Developmental studies of the parasite Vertebrata aterrimophila, showed a unique developmental structure (“trunk-like” cell) not known in other parasites, plus localised infection v and few changes in infected host cells. High-throughput-sequencing revealed mitochondrial genomes of similar size, gene content and order in the parasite Pterocladiophila hemisphaerica to its host Pterocladia lucida, and a reduced non-photosynthetic plastid in the parasite. Mitochondrial (mt) and plastid (cp) genome phylogenies placed Pterocladiophila hemisphaerica on long branches, either as sister to Ceramiales (mt) or Gracilariales (cp). Further analyses, filtering non-elevated plastid genes grouped the parasite neither with the Gracilariales (mt) or Gelidiales (cp) on shorter branches but without support. Nuclear phylogeny grouped P. hemisphaerica as sister to the Gelidiales and other red algal orders and was the only phylogenetic relationship with support. Investigations of photosystem II capacity using PAM fluorometry, and quantifying chlorophyll a content in three pigmented parasites, showed different host nutrient dependencies. Rhodophyllis parasitica and Vertebrata aterrimophila are not able to photosynthesize and are fully dependent on host nutrients. Pterocladiophila hemisphaerica is able to photosynthesize independently, even though it has a reduced non-photosynthetic plastid genome, and therefore is only partially dependent on its host. This study advances our current understanding of red algal parasites and highlights many possibilities for future research including genome evolution and understanding parasite diversity. vi Acknowledgements This PhD thesis would not have been possible without the endless support of my supervisor Joe Zuccarello. I will forever be grateful for the opportunity to do my PhD in your lab. Thanks for taking the time to read my chapters/manuscripts, listening to my presentations and going on fieldtrips and conferences with me etc. Thanks Joe! You have been an amazing supervisor! Another major thanks to my partner Sven Sondhauss. Thanks for all your emotional and financial support. Thanks for always taking care of me when I was sick. I would have never been able to do my PhD without you. Thank you so much for everything. You are the best and I love you! I would also like to thank my secondary supervisor Wendy Nelson for agreeing to supervise my thesis and for always taking the time to support my research, read drafts and go collecting with me. Further thanks go to all the Phycologists in Wellington for all the social gatherings and meetings. It has been a great help and inspiration seeing other scientists balance science and free time. Thanks so much to my family and friends around the world who have supported me constantly during my PhD thesis. Firstly, I would like to thank the hardworking people in KK416 (past and present “now TTR”). Especially, Cong, Kim and Pop! Another thanks to Andrea, Balam, Catherine and Shalen. There have been so many great moments and sometimes tough times during the last three and a half years and I am happy that you could take this journey with me. Thanks to Anna Millek for all the skype talks and messages. Thanks to my godchild Hinemoana, you enriched my life and it is a blessing seeing you grow up. Ein grosser Dank auch an Gerlinde + Eckard Knaup und Frauke + Stefan Sondhauss. I love you heaps guys! Chapter 2: I thank E. K. Ganesan, Yuki Masuda, Narongrit Muangmai, Reinhard Schnetter, Marc Verlaque, and Michael Wynne for publications. I thank two anonymous reviewers and Matt Dring for helpful comments on the manuscript. Chapter 3: This research was supported by a student grant from the Wellington Botanical Society and the Hansjörg Eichler Research Fund from the Australasian Systematic Botany Society. I thank Wendy Nelson for samples and support, Roberta D’Archino (NIWA, Wellington, NZ) for samples and training for hand sectioning and Caoimhghin Ó Maolagáin vii (NIWA, Wellington, NZ) for technical support and the Te Papa museum for access to their herbarium. Chapter 4: Thanks to Wendy Nelson and Roberta D’Archino for access to their microscope facility, Te Papa for access to their herbarium and Andrea Glockner-Fagetti for collection support. Chapter 5: I thank Dan Crossett and Andrea Glockner-Fagetti for diving support. I also thank Chiela Cremen and Chris Jackson for technical support. Chapter 6: Thanks to Ken Ryan for comments on the manuscript and technical support for the experiments. I thank Dan Crossett and Andrea Glockner-Fagetti for scuba diving support and Lisa Woods for statistical consulting. Awards: Thanks to the Australasian Society of Phycology and Aquatic Botany (ASPAB) for selecting my presentation at the ASPAB conference in Hobart, Australia (2015) as the best Macrophyte talk. I thank Victoria University of Wellington for awarding me 3rd place in the SBS Best Student Publication Awards in 2017 for “Red algal parasites: a synopsis of described species, their hosts, distinguishing characters and areas for continued research” (Chapter 2). Conference funding: I would like to also thank the International Phycological Society (IPC) for the P.C. Silva grant and the Australian Society for Phycology and Aquatic Botany (ASPAB) for supporting my attendance at the ASPAB conferences in Hobart (2015) and Warrambool (2016). Another thanks goes to Victoria University of Wellington for the Faculty Strategic Research Grant partial covering my travel costs to the International Phycological Congress in Szczecin, Poland (2017). Laboratory visit: Many thanks to Heroen Verbruggen and his lab for welcoming me warmly during a short laboratory visit in Melbourne and sharing their genomic knowledge with me. General help: Thanks to numerous people, who supported my research as dive and fieldtrip buddies as well as emergency and shore contacts. Thanks to Chris Thorn for always lending a helpful hand. General funding: I thank Victoria University of Wellington for the Victoria Doctoral Fees Scholarship, Victoria Hardship Fund Equity Grants and Victoria Doctoral Submission Scholarship. Examiners: I would like to thank my PhD examiners for reading my PhD thesis and all the helpful comments. viii Thesis declaration I hereby declare that this thesis is my own work and that all sources quoted, paraphrased or otherwise referred to, have been acknowledged in the references at the end of this document. To the best of my knowledge, this thesis neither contains material previously published or written by another person, nor material which to a substantial extent has been accepted for the award of any other degree or diploma of the university or other institutes of higher learning, except where due to the acknowledgement is has been made clear in the text. ix Table of Contents Abstract .....................................................................................................................................
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