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Cell Motility of Early Emerging Apicomplexans

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Cell Motility of Early Emerging Apicomplexans FACULTY OF SCIENCE Cell motility of early emerging apicomplexans Ph.D. Thesis MAGDALÉNA KOVÁČIKOVÁ Supervisor: RNDr. Andrea Bardůnek Valigurová, Ph.D. Department of Botany and Zoology Brno 2019 Bibliographic Entry Author: Mgr. Magdaléna Kováčiková Faculty of Science, Masaryk University Department of Botany and Zoology Title of Thesis: Cell motility of early emerging apicomplexans Degree programme: Biology Specialization: Parasitology Supervisor: RNDr. Andrea Bardůnek Valigurová, Ph.D. Academic Year: 2018/2019 Number of Pages: 278 Keywords: actin; Apicomplexa; archigregarines; α-tubulin; blastogregarines; confocal laser scanning microscopy; electron microscopy; eugregarines; gregarines; motility; myosin; protococcidians; ultrastructure; Western blot Bibliografický záznam Autorka: Mgr. Magdaléna Kováčiková Přírodovědecká fakulta, Masarykova univerzita Ústav botaniky a zoologie Název práce: Buněčná motilita raných linií výtrusovců Studijní program: Biologie Specializace: Parazitologie Vedoucí práce: RNDr. Andrea Bardůnek Valigurová, Ph.D. Akademický rok: 2018/2019 Počet stran: 278 Klíčova slova: aktin; Apicomplexa; archigregariny; α-tubulin; blastogregariny; elektronová mikroskopie; eugregariny; gregariny; konfokální laserová skenovací mikroskopie; motilita; myozin; protokokcídie; ultrastruktura; Western blot Abstract Apicomplexans represent an intensively studied group of unicellular organisms, comprising exclusively of the parasitic genera. Besides significant human and animal pathogens belonging to higher coccidians, Apicomplexa includes several early branching lineages such as protococcidians, blastogregarines and gregarines that are widely dispersed in marine, freshwater and terrestrial invertebrate hosts. Despite apicomplexans enormous diversity, the knowledge of their basal lineages still remains insufficient. Using a combination of experimental, microscopic, biochemical and molecular approaches, the presented thesis describes and compares the motility, subcellular organisation and phylogeny of the poorly investigated lineages of basal apicomplexans. The main aim of thesis was to investigate the cytoskeletal elements (their structure, organisation, nature, and function) responsible for highly diversified motility modes observed in studied marine and terrestrial apicomplexan representatives. The obtained results indicate that these diverse motility modes depend on the modifications of the parasite cell cortex (which is closely interconnected with its parasitism strategies and environment) and differ from substrate-dependent gliding generally described for apicomplexan zoites. In blastogregarines, Siedleckia nematoides performs active pendular/twisting motility similar to the bending/nematode like movement observed in Selenidium archigregarines (S. pygospionis, S. pherusae), while Chattonaria mesnili shows only weak motility with slow and intermittent bending movement. Though blastogregarines and archigregarines are phylogenetically separated groups, they show considerable similarities in their motility patterns and the organisation of their cell cortex with subpellicular microtubules functioning as the main motility motor. Trophozoites and gamonts of both these groups, despite bearing a striking resemblance to overgrown apicomplexan zoites, show no signs of gliding motility. In eugregarines, only the sporozoite stage exhibits the subcellular organisation characteristic of apicomplexan zoites. Ultrastructural study of sporozoites of urosporid eugregarines confirmed the presence of an apical set of organelles and subpellicular microtubules, the structures that are usually not observed at later stages in a majority of eugregarine species. Gliding motility, often accompanied with changes in the cell shape, was observed in eugregarines from terrestrial (Gregarina garnhami, Blabericola cubensis and Protomagalhaensia granulosae from insects) and marine (Polyrhabdina sp. from polychaetes, Cephaloidophora cf. communis from barnacles) hosts. The main leading motor structure in the eugregarine gliding motility appears to be the polymerised form of actin that forms bundles of actin filaments (mostly rib-like myonemes and ectoplasmic network), supported by additional cytoskeletal structures (e.g. specific architecture of epicytic folds and cortical microtubules in some monocystid species) along with secretion of mucopolysaccharides coating the eugregarines surface. In contrast to the above mentioned basal apicomplexans, in protococcidian Eleutheroschizon duboscqi (developing in epicellular position within host-derived parasitophorous sac and sharing the features of gregarines and cryptosporidians) motility was not proven, despite the presence of actin rich subpellicular filaments presumably functioning as the parasite cytoskeleton. Abstrakt Výtrusovci jsou intenzivně zkoumanou skupinou jednobuněčných organismů, zahrnující výlučně parazitické rody. Kromě významných patogenů lidí a zvířat, náležejících do skupiny vyšších kokcidií, Apicomplexa zahrnují několik raných linií, jako jsou protokokcidie, blastogregariny a gregariny, které jsou široce rozšířeny u mořských, sladkovodních a suchozemských bezobratlých. Navzdory obrovské rozmanitosti výtrusovců, jsou znalosti o zástupcích bazálních liniích stále nedostatečné. S využitím kombinovaných experimentálních, mikroskopických, biochemických a molekulárních přístupů předkládaná práce popisuje a porovnává pohyb, subcelulární uspořádaní a fylogenezi u málo prozkoumaných skupin bazálních výtrusovců. Hlavním cílem práce byl výzkum cytoskeletálních struktur (jejich struktury, organizace, charakteru a funkce), zodpovědných za značně rozmanité způsoby pohybu pozorované u studovaných mořských i suchozemských zástupců výtrusovců. Výsledky studie naznačují, že tyto rozmanité způsoby pohybu závisí od modifikací buněčného kortexu parazita (který je úzce spjat se strategiemi parazitismu a životním prostředím parazita) a liší se od klouzavého, na substrátu závislého pohybu, obecně popsaného u zoitů výtrusovců. V případě blastogregarin, Siedleckia nematoides vykazuje aktivní kyvadlový/kroutivý pohyb podobný ohýbavému pohybu hlístic, pozorovanému u archigregarin rodu Selenidium (S. pygospionis, S. pherusae), zatímco Chattonaria mesnili vykazuje jen nevýrazný pohyb ve formě pomalého a přerušovaného ohýbání. I když jsou blastogregariny a archigregariny řazeny do různých fylogenetických skupin, vykazují značnou podobnost ve způsobu pohybu a v morfologii buněčného kortexu, kde subpelikulární mikrotubuly představují hlavní motor pohybu. Trofozoiti a gamonti obou skupin, navzdory jejich výrazné podobnosti s hypertrofovanými zoitmi výtrusovců, nevykazují žádné známky klouzavého pohybu. U eugregarin byla subcelulární organizace shodná se zoitmi výtrusovců pozorována pouze ve stadiu sporozoita. Ultrastrukturální výzkum sporozoitů urosporidních eugregarin potvrdil přítomnost apikálních organel a mikrotubulů, struktur, které obvykle nejsou pozorovány u pozdních stadií většiny eugregarin. Klouzavý pohyb, ve většině případů spojen se změnou buněčného tvaru, byl pozorován u eugregarin ze suchozemských (Gregarina garnhami, Blabericola cubensis a Protomagalhaensia granulosae z hmyzu) jako i mořských (Polyrhabdina sp. z mnohoštětinatců, Cephaloidophora cf. communis ze svijonožců) hostitelů. Hlavní strukturou zabezpečující pohyb u klouzajících druhů eugregarin se jeví být aktin ve své polymerizované formě, tvořící provazce aktínových vláken (především žebrovité myonémy a ektoplasmatickú síť vláken), spolu s přídavnými cytoskeletálními strukturami (např. specifická stavba záhybů epicytu či kortikální mikrotubuly u některých monocystidních druhů) a sekrecí mukopolysacharidů pokrývajících povrch gregarin. Na rozdíl od výše zmiňovaných bazálních skupin výtrusovců, u protokokcídie druhu Eleutheroschizon duboscqi (vyvíjející se epicelulárně v parazitiformním vaku odvozeným z hostitelské buňky a sdílející charakteristiky gregarin i kryptosporidií) pohyb nebyl prokázán, i přes přítomnost subpelikulárních filamentů bohatých na aktin, pravděpodobně majících funkci jako cytoskelet parazita. Acknowledgements I am very grateful to my supervisor Dr. Andrea Bardůnek Valigurová for her valuable advice and consultations, as well as for managing many of the practical aspects of this study and helping me with samples evaluations and interpretations. I also would like to thank Assoc. Prof. Milan Gelnar, who gave me an opportunity to work on parasitic protist and financially supported this research. Many thanks to my colleagues and co-authors from different scientific institutions, namely Dr. Andrei Dakin, Dr. Naděžda Vaškovicová, Assoc. Prof. Gita G. Paskerova, Assoc. Prof. Timur G. Simdyanov and Prof. Isabelle Florent, for sharing their valuable knowledge and for the opportunity to work in their laboratories. I am very grateful for the support from the Department of Botany and Zoology, Faculty of Science, Masaryk University, towards my study. I would also like to thank the staff of the White Sea Biological Station of Lomonosov Moscow State University for help with material obtaining and to the members of Laboratory of Electron Microscopy, Biology Centre Czech Academy of Science for assistance in obtaining the electron microscopic data. Finally, I would like to express my gratitude to my family and friends for their ongoing support and encouragement in helping me to complete this work. Financial support for this study was provided by the Czech Science Foundation, project No. GBP505/12/G112 (ECIP - Centre of excellence). Travel expenses
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