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Evolution of the Heme Biosynthetic Pathway in Eukaryotic Phototrophs

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Evolution of the Heme Biosynthetic Pathway in Eukaryotic Phototrophs School of Doctoral Studies in Biological Sciences University of South Bohemia in České Budějovice Faculty of Science Evolution of the Heme Biosynthetic Pathway in Eukaryotic Phototrophs Ph.D. Thesis Mgr. Jaromír Cihlář Supervisor: Prof. Ing. Miroslav Oborník, Ph.D. Biology Centre CAS v.v.i., Institute of Parasitology České Budějovice 2018 This thesis should be cited as: Cihlář J., 2018. Evolution of the Heme Biosynthetic Pathway in Eukaryotic Phototrophs. Ph.D. Thesis Series, University of South Bohemia, Faculty of Science, School of Doctoral Studies in Biological Sciences, České Budějovice, Czech Republic. Annotation This thesis is devoted to the evolution of the heme biosynthetic pathway in eukaryotic phototrophs with particular emphasis on algae possessing secondary and tertiary red and green derived plastids. Based on molecular biology and bioinformatics approaches it explores the diversity and similarities in heme biosynthesis among different algae. The core study of this thesis describes the heme biosynthesis in Bigelowiella natans and Guillardia theta, algae containing a remnant endosymbiont nucleus within their plastids, in dinoflagellates containing tertiary endosymbionts derived from diatoms – called dinotoms, and in Lepidodinium chlorophorum, a dinoflagellate containing a secondary green plastid. The thesis further focusses on new insights in the heme biosynthetic pathway and general origin of the genes in chromerids the group of free-living algae closely related to apicomplexan parasites. Declaration [in Czech] Prohlašuji, že svoji disertační práci jsem vypracoval samostatně pouze s použitím pramenů a literatury uvedených v seznamu citované literatury. Prohlašuji, že v souladu s § 47b zákona č. 111/1998 Sb. v platném znění souhlasím se zveřejněním své disertační práce, a to v nezkrácené podobě elektronickou cestou ve veřejně přístupné části databáze STAG provozované Jihočeskou univerzitou v Českých Budějovicích na jejích internetových stránkách, a to se zachováním mého autorského práva k odevzdanému textu této kvalifikační práce. Souhlasím dále s tím, aby toutéž elektronickou cestou byly v souladu s uvedeným ustanovením zákona č. 111/1998 Sb. zveřejněny posudky školitele a oponentů práce i záznam o průběhu a výsledku obhajoby kvalifikační práce. Rovněž souhlasím s porovnáním textu mé kvalifikační práce s databází kvalifikačních prací Theses.cz provozovanou Národním registrem vysokoškolských kvalifikačních prací a systémem na odhalování plagiátů. České Budějovice, 19.01.2018 ............................. Jaromír Cihlář This thesis originated from a partnership of Faculty of Science, University of South Bohemia, and Institute of Parasitology, Biology Centre CAS v.v.i., supporting doctoral studies in the Molecular biology and genetics study program. Financial support This work was financially supported by following grants and supporting institutions: Grant Agency of the Czech Republic project P501-12-G055 Grant Agency of the Czech Republic project 15-17643S Grant Agency of the Czech Republic project P506-12-1522 Acknowledgements: I would like to express my immense gratitude to my supervisor Miroslav Oborník for giving me the opportunity to work on such an interesting topic. I sincerely appreciate his enthusiasm, support, and last but not least his patient guidance. I would also like to thank all the members of Laboratory of Evolutionary Protistology for their inspiring advices, help, and especially for being always great colleagues. My special thanks belong to Zoltán Füssy for excellent collaboration and for proofreading. Furthermore, I would like to express many thanks to my beloved Olinka for her love, patience and support. I am immensely thankful to my family: my mother, father and my grandmother for their constant faith in me and for the support of all kinds. List of papers and author’s contribution The thesis is structured based on the following papers: Cihlář J, Füssy Z, Horák A, Oborník M. (2016) Evolution of the Tetrapyrrole Biosynthetic Pathway in Secondary Algae: Conservation, Redundancy and Replacement. PLOS One 11(11):e0166338. J. Cihlář and Z. Füssy contributed equally to this work. Jaromír performed heme pathway in silico targeting predictions and phylogenetic analyses of B. natans and G. theta, and participated in production of visualizations, writing and reviewing the manuscript. Woo YH, Ansari H, Otto TD, Klinger CM, Kolisko M, Michálek J, Saxena A, Shanmugam D, Tayyrov A, Veluchamy A, Ali S, Bernal A, del Campo J, Cihlář J, Flegontov P, Gornik SG, Hajdušková E, Horák A, Janouškovec J, Katris NJ, Mast FD, Miranda-Saavedra D, Mourier T, Naeem R, Nair M, Panigrahi AK, Rawlings ND, Padron-Regalado E, Ramaprasad A, Samad N, Tomčala A, Wilkes J, Neafsey DE, Doerig C, Bowler C, Keeling PJ, Roos DS, Dacks JB, Templeton TJ, Waller RF, Lukeš J, Oborník M, Pain A. (2015) Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites. eLife 4:e06974. J. Cihlář performed DNA and RNA extractions, library preparation and sequencing, and heme pathway in silico targeting predictions and phylogenetic analyses. Burki F, Flegontov P, Oborník M, Cihlář J, Pain A, Lukeš J, Keeling PJ. (2012) Re- evaluating the green versus red signal in eukaryotes with secondary plastid of red algal origin. Genome Biology Evolution 4(6):626-35. J. Cihlář participated in the identification of contamination by higher plant sequences, and with M. Oborník in the evaluation of phylogenies. Miroslav Oborník, the supervisor of this Ph.D. thesis and co-author of all presented papers, approves the contribution of Jaromír Cihlář in these papers as described above. ……………..……………………………………… Prof. Ing. Miroslav Oborník, Ph.D. Table of contents Review ............................................................................................................................ 1 Evolution of the heme biosynthetic pathway in eukaryotic phototrophs 1 Introduction ............................................................................................................. 1 1.1 Importance of heme in living organisms ......................................................... 2 2 Biosynthesis of heme .............................................................................................. 4 2.1 Biosynthesis of heme in eukaryotes and the significance of the endosymbiotic gene transfer ........................................................................... 5 2.2 Biosynthesis of heme in primary heterotrophs ................................................ 6 2.3 Biosynthesis of heme in phototrophic eukaryotes ........................................... 7 2.3.1 Primary phototrophs ............................................................................... 7 2.3.2 Other phototrophs ................................................................................ 13 2.3.2.1 Biosynthesis of heme in algae with secondary and tertiary plastids derived from the red lineage ........................................... 15 2.3.2.2 Biosynthesis of heme in algae with secondary plastids derived from the green lineage ................................................................. 21 3 Conclusion ............................................................................................................ 25 References .............................................................................................................. 26 Paper I .......................................................................................................................... 39 Evolution of the Tetrapyrrole Biosynthetic Pathway in Secondary Algae: Conservation, Redundancy and Replacement Paper II ..................................................................................................................................... 70 Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites Paper III .................................................................................................................................. 112 Re-evaluating the green versus red signal in eukaryotes with secondary plastid of red algal origin Final conclusion ........................................................................................................ 123 Curriculum vitae ........................................................................................................ 126 Evolution of the heme biosynthetic pathway in eukaryotic phototrophs Jaromír Cihlář Faculty of science, University of South Bohemia; Institute of Parasitology, Biology centre ASCR, České Budějovice, Czech Republic. Abstract: Tetrapyrroles such as heme and chlorophyll are involved in energy consumption (oxidative phosphorylation) and fixation (photosynthesis) and therefore are crucial components for cell metabolism. Biosynthetic pathway responsible for tetrapyrrole production is present in all three domains of cellular life. In eukaryotes, the pathway was shaped by past endosymbioses and consecutive endosymbiotic and non-endosymbiotic gene transfers which turned it into a true mosaic of enzymes with diverse origins and often with different subcellular localization. This thesis discusses the current view on the heme biosynthesis in eukaryotic phototrophs, how the pathway evolved during the history of plastid endosymbioses and how it adapted in response to evolutionary events. 1 Introduction Tetrapyrrole biosynthetic pathway is undoubtedly one of the most important enzymatic pathways in living organisms. Besides
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