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Genomics of Blastocrithidia, a Trypanosomatid with All Three Stop Codons Reassigned

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Genomics of Blastocrithidia, a Trypanosomatid with All Three Stop Codons Reassigned Biology Centre, Institute of Parasitology, Czech Academy of Sciences, and University of South Bohemia, Faculty of Sciences, České Budějovice, Czech Republic Ph.D. Thesis Genomics of Blastocrithidia, a trypanosomatid with all three stop codons reassigned Anna Nenarokova, MSc Supervisor: Prof. RNDr. Julius Lukeš, CSc. České Budějovice, 2020 This thesis should be cited as: Nenarokova A., 2019: Genomics of Blastocrithidia, a trypanosomatid with all three stop codons reassigned. Ph.D. thesis. University of South Bohemia, Faculty of Science, School of doctoral studies in biological sciences, České Budějovice, Czech Republic. Annotation This work describes genomic studies of Blastocrithidia, the trypanosomatid with all three stop codons encoding amino acids and the only known euglenozoan with non-standard nuclear genetic code. We describe unique genomic features of Blastocrithidia and the sister clade "Jaculum", and discuss possible mechanisms of translation termination with ambiguous stop codons and the evolutionary path that may have established this system. Declaration I hereby declare that I did all the work presented in this thesis by myself or in collaboration with the mentioned co-authors and only using the cited literature. České Budějovice, .............................................................................................. Anna Nenarokova 2 Prohlášení Prohlašuji, že svoji disertační práci jsem vypracovala 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 úpravě vzniklé vypuštěním vyznačených částí archivovaných Přírodovědeckou fakultou 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. V Českých Budějovicích dne ______________, Anna Nenarokova ____________________ 3 This thesis originated from a partnership between the Faculty of Science, University of South Bohemia, and Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, supporting doctoral studies in the Molecular and Cell biology and Genetics study program. Financial support This work was supported by the Czech Grant Agency (15–21974S and 16–18699S), the ERC CZ grant (LL1601), the Czech Ministry of Education (ERD Funds OPVVV16_019/ 0000759). 4 Acknowledgements First of all, I wish to sincerely thank my supervisor Julius Lukeš III for believing in me, his patience and support through my Ph.D. studies. I admire his courage and boldness, endless life force and enthusiasm. Next, I would like to thank my colleagues and collaborators on the Blastocrithidia project: Kika Záhonová, who is the first author of the original Blastocrithidia paper and did a significant part of the bioinformatic work of the current project; Serafim Nenarokov, who developed the annotation software and has been helping me in many other ways; Ambar Kachale, who did most of the experimental work; Zdeněk Paris, who is our advisor for the tRNA part of the project and performed some of the tRNA experiments; Míša Svobodová, who prepared the RNAi cell lines of genuine and putative cytidine deaminases of T. brucei; Eva Horáková, who is one of our advisors for experimental part of the project; Jan Votýpka and Alexey Kostygov, who provided the cultures of Blastocrithidia sp. and “Jaculum”; Juan Alfonzo for useful discussions; Slava Yurchenko, who is a co-supervisor of the project and contributed a lot of high-quality sequence data; Marek Eliáš, who is the senior author of the original Blastocrithidia paper and who shared with us many smart and useful ideas. Besides, I want to thank Ambar Kachale and Míša Svobodová for their help with the description of the experimental part of the work. I am very grateful to other members of the TriTryp labs and my other colleagues from the Institute of Parasitology who were very friendly and helped me in many ways. Also, I want to express my gratitude to Drs. Tom Williams and Celine Petitjean from the University of Bristol for taking me to practice in their laboratory, being very friendly and welcoming to me, and sharing with me their experience and knowledge. Last, but not least, I would like to thank all my friends and loved ones who stood on my side, who took care of me in my lowest moments, when I felt down and desperate. Without their help and support I would not get here. 5 List of publications and author’s contribution Publications listed chronologically: 1. Kostygov A.Y., Butenko A., Nenarokova A., Tashyreva D., Flegontov P., Lukeš J. and Yurchenko V. (2017) Genome of Ca. Pandoraea novymonadis, an endosymbiotic bacterium of the trypanosomatid Novymonas esmeraldas. Front. Microbiol. 8:1940. doi:10.3389/fmicb.2017.01940 Anna Nenarokova assembled and annotated the genomes of Novymonas esmeraldas and its symbiont Ca. Pandoraea novymonadis and contributed to the interpretation of data. 2. Zíková A., Verner Z., Nenarokova A., Michels P.A.M., Lukeš J. (2017). A paradigm shift: The mitoproteomes of procyclic and bloodstream Trypanosoma brucei are comparably complex. PLoS Path. 13 (12), e1006679. doi:10.1371/journal.ppat.1006679 Anna Nenarokova participated in the data preparation and analysis. 3. Schwelm A., Badstöber J., Bulman S., Desoignies N., Etemadi M., Falloon R. E., Gachon C. M. M., Legreve A., Lukeš J., Merz U., Nenarokova A., Strittmatter M., Sullivan B. K. and Neuhauser S. (2018) Not in your usual Top 10: protists that infect plants and algae. Molecular Plant Pathology. doi:10.1111/mpp.12580 Anna Nenarokova wrote the chapter about the genus Phytomonas in this review. 4. Harmer J., Yurchenko V., Nenarokova A., Lukeš J., Ginger M.L. (2018). Farming, slaving and enslavement: histories of endosymbioses during kinetoplastid evolution. Parasitology 145, 1311–1323. doi:10.1017/S0031182018000781 Anna Nenarokova participated in the data preparation and analysis. 5. Ebenezer T., Zoltner M., Burrel A., Nenarokova A., Novák Vanclová A.M.G., Prasad B., Soukal P., Santana-Molina C., O’Neill E., Nankissoor N.N., Vadakedath N., Daiker V., Obado S., Jackson A.P., Devos D., Lukeš J., Lebert M., Vaughan S., Hampl V., 6 Carrington M., Ginger M.L., Dacks J.B., Kelly S., Field M.C. (2018). Transcriptome, proteome and draft genome of Euglena gracilis. BMC Biology 17 (1), 11. doi:10.1186/s12915-019-0626-8 Anna Nenarokova predicted in silico the mitochondrial proteome of Euglena gracilis, functionally annotated mitochondrial proteins and pathways, and wrote the chapter about mitochondrial proteins. 6. Nenarokova A., Záhonová K., Krasilnikova M., Gahura O., McCulloch R., Zíková A., Yurchenko V., Lukeš J. (2019). Causes and effects of loss of classical nonhomologous end joining pathway in parasitic eukaryotes. mBio 10 (4), e01541-19. doi:10.1128/mBio.01541-19. Anna Nenarokova conceived and designed the study, performed most of the data analysis, and wrote most of the article. 7. Kosakyan A., Alama-Bermejo G., Bartošová-Sojková P., Born-Torrijos A., Šíma R., Nenarokova A., Eszterbauer E., Bartholomew J., Holzer A.S. (2019). Selection of suitable reference genes for gene expression studies in myxosporean (Myxozoa, Cnidaria) parasites. Scientific Reports. 9(1):15073. doi:10.1038/s41598-019-51479-0. Anna Nenarokova helped with the transcriptome assembly, filtering and analysis. 8. Hammond M.J., Nenarokova A., Butenko A., Zoltner M., Lacová Dobáková E., Field M.C., Lukeš J. A uniquely complex mitochondrial proteome from Euglena gracilis. Re- submitted to Molecular Biology and Evolution. Anna Nenarokova made the initial bulk functional annotation of MS-MS determined proteins from the E. gracilis mitochondrial fraction, assigned them to functional modules and reconstructed mitochondrial pathways, and participated in data analysis and interpretation. Moreover, she wrote the chapter “RNA editing and processing”. Prof. RNDr. Julius Lukeš, CSc. ____________________ 7 Table of contents Preface 11 My role in the Blastocrithidia project 12 Structure of the thesis 12 1 Introduction 13 1.1.1 Blastocrithidia phylogenetic position, evolution and systematics 13 1.2 Gene expression in kinetoplastids 16 1.2.1 Genome organization, transcription and trans-splicing 16 1.2.2 Post-transcriptional events and translation in kinetoplastids 19 1.3 Evolution and variations of genetic code 20 1.3.1 Standard genetic code and its origin 20 1.3.2 Non-standard genetic codes in nature 21 1.3.3 Codon reassignment theories 23 1.3.4 Translation termination and stop codon reassignment 25 1.3.5 Organisms with all three stop codons reassigned 27 1.3.6 Genetic code in kinetoplastids 28 2 Materials and Methods 30 2.1 Cell cultures 30 2.2 Poisoned primer extension 30 2.3 RNAi of T. brucei cytidine deaminase candidate genes 31 2.4 Genome and transcriptome sequencing, assembly and mapping 31 2.5 Mass spectrometry analysis 32 2.6 BLAST searches, alignments 33 2.7 Genome annotation 33 2.8 tRNA prediction and analysis 34 8 2.9 Codon usage 34 3 Results and Discussion 35 3.1 Genome statistics 35 3.2 Translation termination in Blastocrithidia 36 3.2.1 Defining the genuine stop codon 36 3.3 Potential mechanisms of translation termination in Blastocrithidia 38 3.4 Codon usage 40 3.4.1 Codon usage and GC content 40 3.4.2 Usage of the reassigned stop codons 41 3.5 tRNAs 45 3.6 NMD is absent in the Blastocrithidia clade 51 3.7 Insertions and DNA repair in Blastocrithidia and other trypanosomatids 53 4 Summary 54 4.1 Hypotheses about the evolutionary path of Blastocrithidia 54 4.2 Conclusions and perspectives 55 5 References 56 6 Supplementary information 73 Figure S1.
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