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Parasitology Mgr. Anna Novák Vanclová Evolution of Euglenid

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Parasitology Mgr. Anna Novák Vanclová Evolution of Euglenid Charles University, Faculty of Science Univerzita Karlova, Přírodovědecká fakulta Study program: Parasitology Studijní program: Parazitologie Mgr. Anna Novák Vanclová Evolution of euglenid plastid proteome Evoluce proteomu plastidu euglenidů Doctoral thesis Thesis supervisor: doc. Vladimír Hampl, Ph.D. Prague, 2019 Declaration of the author: I declare that I elaborated this thesis independently. I also proclaim that the literary sources were cited properly and neither this work nor a substantial part of it has been used to obtain the same or any other academic degree. Prohlašuji, že jsem tuto práci zpracovala samostatně a že jsem uvedla všechny použité zdroje a literaturu. Tato práce ani její podstatná část nebyla předložena k získání jiného nebo stejného akademického titulu. Mgr. Anna Novák Vanclová 2 Declaration of the thesis supervisor: Data presented in this thesis are the result of team collaboration at the Laboratory of evolutionary protistology and cooperation with external associates at the University of Dundee and University of Ostrava. I declare that the involvement and contribution of Anna Novák Vanclová in this work was substantial and sufficient in terms of scope and quality for the award of doctoral degree. doc. Vladimír Hampl, Ph.D. Thesis supervisor 3 Acknowledgements I would like to give many thanks to my supervisor Vladimír Hampl for sparking my interest in evolutionary protistology in 2010 and for the following years of his support, encouragement, and guidance. Thanks also to my labmates and other colleagues from near and far for their advice and goodwill. Special thanks to Martin Vancl, my brother who was always there to help, and Lukáš Novák, a partner in both science and life who unfailingly supported me through thick and thin. 4 Table of contents ABSTRACT ............................................................................................................................... 7 ABSTRAKT ............................................................................................................................... 8 1 INTRODUCTION .............................................................................................................. 9 1.1 Euglenophyta .............................................................................................................. 9 1.1.1 Evolutionary position and general characteristics ................................................ 9 1.1.2 Morphology and cell structure ............................................................................. 9 1.1.3 Diversity, distribution and ecological significance ............................................ 11 1.1.4 Euglena gracilis as a model euglenophyte ......................................................... 12 1.1.4.1 Genome and gene expression ...................................................................... 12 1.1.4.2 Genetic tools ............................................................................................... 13 1.2 Plastids ..................................................................................................................... 13 1.2.1 The origin of plastids .......................................................................................... 13 1.2.1.1 Primary endosymbiosis and related phenomena ......................................... 13 1.2.1.2 Secondary and higher endosymbioses ........................................................ 14 1.2.1.3 The origin of euglenid plastids ................................................................... 16 1.2.2 Plastid membranes and general structure ........................................................... 17 1.2.2.1 Primary plastids .......................................................................................... 17 1.2.2.2 Complex plastids ......................................................................................... 18 1.2.2.3 Euglenid plastids ......................................................................................... 18 1.2.3 Plastid genomes and genetic housekeeping ....................................................... 19 1.2.3.1 Primary plastids .......................................................................................... 19 1.2.3.2 Complex plastids ......................................................................................... 20 1.2.3.3 Euglenid plastids ......................................................................................... 21 1.2.4 Plastid biogenesis ............................................................................................... 22 1.2.4.1 Primary plastids .......................................................................................... 23 1.2.4.2 Complex plastids ......................................................................................... 26 1.2.4.3 Euglenid plastids ......................................................................................... 28 1.2.5 Metabolic functions of plastids .......................................................................... 31 1.2.5.1 Primary plastids .......................................................................................... 31 1.2.5.2 Complex plastids ......................................................................................... 35 5 1.2.5.3 Euglenid plastids ......................................................................................... 39 1.3 Plastid proteomics .................................................................................................... 41 1.3.1 General methods in proteomics .......................................................................... 41 1.3.2 Plastid proteomes ............................................................................................... 42 2 AIMS ................................................................................................................................ 44 3 LIST OF PUBLICATIONS AND AUTHOR CONTRIBUTION ................................... 45 4 SUMMARY ..................................................................................................................... 46 5 REFERENCES ................................................................................................................. 50 6 PUBLICATIONS ............................................................................................................. 70 6 ABSTRACT Endosymbiotic gain and transfer of plastids is a widespread evolutionary phenomenon and a major driving force of eukaryotic evolution. The integration of a new organelle is accompanied by changes in its structure, gene content, molecular mechanisms for biogenesis and transport, and re-wiring of the host and organelle metabolic pathways. To understand the course and underlying mechanisms of plastid evolution, it is important to study these processes in variety of secondary algae and notice their differences and similarities. Euglenophytes gained their plastids from green eukaryotic algae after a long history of heterotrophic lifestyle. In my thesis, I participated in analyses of newly generated sequence datasets: transcriptomes of Euglena gracilis and Euglena longa and mass spectrometry-determined proteome of E. gracilis plastid with especial regard to the potential novelties associated with plastid gain and incorporation. In the resulting publications we particularly focus on plastid protein import machinery and targeting signals and report extremely reduced TIC and completely absent TOC in euglenophyte plastid. Using the proteomic dataset, we predict potential novel plastid protein translocases recruited from ER/Golgi and re-analyze plastid signal domains, characterizing previously overlooked features. Protein inventory of E. gracilis plastid suggests complex, in some cases redundant metabolic capacity. Chlorophyll recycling is one of the sources of phytol for reactions not connected to MEP/DOXP pathway. Plastid contribution to amino acid metabolism is very low, if any. We screen the proteome for proteins of other than green algal phylogenetic affiliation and report substantial contribution from “chromists” as well as several cases of LGT from bacteria, including an acquisition of additional SUF pathway. In summary, the work presented in this thesis provides a solid contribution to plastid proteomics, resource for both basic and applied Euglena research and potential foundation for various follow-up studies. 7 ABSTRAKT Vznik plastidů endosymbiózou a jejich horizontální šíření je široce rozšířený evoluční jev a jedna z významných hnacích sil evoluce eukaryot. Integrace nové organely je doprovázena změnami v její struktuře, genovém obsahu, biogenezi a importu proteinů a propojením jejích metabolických drah s drahami hostitele. Studium těchto procesů v různých skupinách sekundárních řas a srovnávání mezi nimi je důležité pro porozumění obecným principům evoluce plastidů. Krásnoočka (Euglenophyta) získala své plastidy od zelených řas po poměrně dlouhém období heterotrofie. V této práci jsem se podílela na analýze nově vygenerovaných sekvenčních datasetů: transkriptomů Euglena gracilis a Euglena longa a plastidového proteomu E. gracilis determinovaného pomocí hmotnostní spektrometrie, a to s ohledem na potenciální inovace související se získáním a integrací plastidu. Ve výsledných publikacích jsme se zaměřili zvláště na složení a evoluci systému pro targeting a import jaderně kódovaných proteinů do plastidu a zjistili, že plastidy krásnooček obsahují extrémně redukovaný TIC a zcela postrádají TOC komplex.
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