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Of Mitochondria: Investigating the Functioning, Maintenance and Evolutionary Relevance of a Naturally Heteroplasmic System

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Université de Montréal Energy metabolism in species with Doubly Uniparental Inheritance (DUI) of mitochondria: investigating the functioning, maintenance and evolutionary relevance of a naturally heteroplasmic system Par Stefano Bettinazzi Département de sciences biologiques, Faculté des arts et des sciences Thèse présentée en vue de l’obtention du grade de Philosophiae Doctor (Ph.D.) en sciences biologiques June 2020 © Stefano Bettinazzi, 2020 A été évaluée par un jury composé des personnes suivantes Sandra Binning Président-rapporteur Sophie Breton Directeur de recherche Pierre Blier Codirecteur Annie Anger Membre du jury Ron Burton Examinateur externe RÉSUMÉ Les mitochondries et leur génome, l'ADN mitochondrial (ADNmt), sont généralement transmis uniquement par la mère aux fils et aux filles chez les métazoaires (transmission strictement maternelle, SMI). Une exception à la règle générale de la SMI se trouve dans environ 100 espèces de bivalves, qui se caractérise par une double transmission uniparentale (DUI) des mitochondries. Chez les espèces DUI, deux lignées d'ADNmt très divergentes et liées au sexe coexistent. Une lignée mitochondriale maternelle (type F), présente dans les ovocytes et les tissus somatiques des individus femelles et males, et une lignée paternelle (type M), présente dans les spermatozoïdes. Dans les tissus somatiques mâles, les deux lignées coexistent parfois, une condition appelée hétéroplasmie. En sachant que les variations génétiques dans l’ADNmt peuvent avoir un impact sur les fonctions mitochondriales, et en donnant l'association stricte des ADNmt de type M et F avec différents gamètes, il est imaginable que la forte divergence entre les deux lignées DUI puisse entraîner des adaptations bioénergétiques avec répercussion sur la reproduction. Le système DUI apporte également la nécessité pour les mitochondries paternelles de préserver leur propre intégrité génétique, ainsi que pour les cellules somatiques de faire face à l'hétéroplasmie. L'objectif de ma thèse était de lier le génotype mitochondrial des espèces bivalves DUI et SMI au phénotype. Plus précisément, j'ai exploré l'impact des variations de l'ADN mitochondrial spécifiques au sexe sur un large éventail de traits phénotypiques, allant de la bioénergétique mitochondriale et cellulaire à la performance des spermatozoïdes, en étudiant la valeur adaptative du système DUI à la lumière du fitness reproductif, de la sélection et de la transmission mitochondriales. Les résultats issus de ce projet de thèse ont révélé une nette divergence phénotypique entre les espèces DUI et SMI, reflétant peut-être les différentes pressions sélectives agissant sur les deux lignées mitochondriales. Contrairement aux espèces SMI, l'évolution sexo-spécifique des variants d'ADNmt DUI entraîne l'expression de différents phénotypes bioénergétiques mâles et femelles. Au niveau de la fonctionnalité mitochondriale, les mitochondries DUI de type M présentent une phosphorylation oxydative (OXPHOS) remodelée, caractérisée par un contrôle respiratoire inhabituel à l'extrémité de la chaîne respiratoire. La réorganisation générale de la bioénergétique des spermes DUI entraîne également une variation de l'équilibre entre les principales voies de production d'énergie, incluant la glycolyse, la glycolyse anaérobique, le métabolisme des acides gras, le cycle de l'acide tricarboxylique, l'OXPHOS, ainsi que la capacité antioxydante. Enfin, les spermatozoïdes DUI comptent entièrement sur l'énergie produite par OXPHOS pour maintenir une motilité inhabituelle caractérisée par une vitesse lente et une trajectoire plus curviligne, traits potentiellement associés à un plus grand succès de reproduction chez les organismes marins sessiles. Aussi, ils conservent la capacité de passer à une stratégie de production d'énergie mixte (aérobique et anaérobie) après la détection des ovocytes. Dans l'ensemble, ces résultats suggèrent que la variation de l'ADNmt dans les espèces DUI pourrait être adaptative, incluant adaptation bioénergétique sexo-spécifiques avec un effet en aval sur la performance des spermatozoïdes, la capacité de reproduction, la sélection et transmission des mitochondries paternelles. Mots-clés: mitochondries - DUI - SMI - bivalves - gamètes - hétéroplasmie - OXPHOS - métabolisme énergétique - coévolution mitonucléaire 6 ABSTRACT Mitochondria and their genome, the mitochondrial DNA (mtDNA), are usually transmitted only by the mother to both sons and daughters in metazoan (i.e. strict maternal inheritance, SMI). An exception to the general rule of SMI is found in around 100 species of bivalves, which are characterized by a doubly uniparental inheritance (DUI) of mitochondria. In DUI species, two highly divergent and sex-linked mtDNA lineages coexist. One mitochondrial lineage is maternally inherited (F-type) and is present in oocytes and somatic tissues of both female and male individuals. The other lineage is paternally inherited (M-type) and is present in sperm. In male somatic tissues both lineages sometimes coexist, a condition named heteroplasmy. Knowing that variations in mitochondrially-encoded genes might impact mitochondrial functions, and giving the strict association of M and F-type mtDNAs with different gametes, it is conceivable that the variation between the two DUI lineages might result in sex-specific bioenergetic adaptations with repercussion on reproduction. Despite providing an unprecedented opportunity for the mtDNA to evolve for male functions, the DUI system also brings the need for sperm mitochondria to preserve their genetic integrity, as well as for somatic cells to deal with heteroplasmy. The objective of my PhD was to link the mitochondrial genotype of DUI and SMI bivalve species to the phenotype. I explored the impact of sex-specific mtDNA variations upon a wide set of phenotypic traits, ranging from mitochondrial and cellular bioenergetics to sperm performance, investigating the adaptive value of DUI system in the light of reproductive fitness, mitochondrial selection, preservation and transmission. The results stemming from this PhD project revealed a clear phenotypic divergence between DUI and SMI species, possibly reflecting the different selective pressures acting on their mitochondria as a result of their different mode of mitochondria transmission. Conversely to SMI species, the sex-specific evolution of DUI mtDNA variants results in the expression of different male and female bioenergetic phenotypes. At the level of mitochondrial functionality, M-type mitochondria exhibit a remodelled OXPHOS characterized by unusual respiratory control at the terminus of the respiratory chain. The general reorganization of DUI sperm bioenergetics also entails variation in the balance between the main energy producing pathways, including glycolysis, anaerobic glycolysis, fatty acid metabolism, tricarboxylic acid cycle, OXPHOS, as well as the antioxidant capacity. Finally, DUI sperm exhibit an unusual motility phenotype characterized by slow speed and high curvilinear trajectory, traits potentially associated with a higher reproductive success in sessile broadcast spawning marine organisms. They also completely rely on the energy produced by OXPHOS to sustain their performance, although maintaining the ability to switch to a more combined aerobic/anaerobic strategy of energy production after oocyte detection. Altogether, these results suggest that the mtDNA variation in DUI species might be adaptive, resulting in the expression of sex-specific bioenergetic adaptation with downstream effect on sperm performance, reproductive fitness, paternal mitochondria selection, preservation and transmission. The results also suggest that heteroplasmy has an impact onto the bioenergetics of male soma, and that a functional compensation between genomes might minimize any potential deleterious outcome. Keywords: mitochondria – DUI – SMI – bivalves – gametes – heteroplasmy – OXPHOS – energy metabolism – mitonuclear coevolution 8 Table of contents RÉSUMÉ .......................................................................................................................................... 5 ABSTRACT ..................................................................................................................................... 7 Table of contents .............................................................................................................................. 9 List of tables ................................................................................................................................... 13 List of figures ................................................................................................................................. 19 List of acronyms and abbreviations ............................................................................................... 27 Acknowledgements ........................................................................................................................ 35 CHAPTER I – GENERAL INTRODUCTION ............................................................................. 37 Mitochondria, a cellular power plant ......................................................................................... 37 A small but valuable genome, the mitochondrial DNA ......................................................... 39 Mitonuclear coevolution ............................................................................................................ 41 Cytonuclear incompatibility ..................................................................................................
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  • Nuttallia Brasiliensis E Theileria Brasiliensis, Sinonímias De Babesia Brasiliensis (Piroplasmida: Babesiidae) Hemoparasito De Marsupiais Didelphidae

    Nuttallia Brasiliensis E Theileria Brasiliensis, Sinonímias De Babesia Brasiliensis (Piroplasmida: Babesiidae) Hemoparasito De Marsupiais Didelphidae

    Parasitol Latinoam 58: 89 - 91, 2003 FLAP COMENTARIO TAXONÓMICO Nuttallia brasiliensis e Theileria brasiliensis, sinonímias de Babesia brasiliensis (Piroplasmida: Babesiidae) hemoparasito de marsupiais Didelphidae MARCELLO XAVIER SAMPAIO* e CARLOS LUIZ MASSARD** Nuttallia brasiliensis AND Theileria brasiliensis, SYNONYM OF Babesia brasiliensis (PIROPLASMIDA: BABESIIDAE) HEMOPARASITE OF MARSUPIALS Transference of the South American opossums hemoparasite Nuttallia brasiliensis to the genus Babesia are discussed and proposed due to the pre-occupation of Nuttallia genus by mollusk species, as well as the synonym of Theileria brasiliensis to Babesia brasiliensis. Simultaneously the situation of the others members of Nuttallia and Achromaticus genus is discussed, in relation with the international rules of nomenclature and its common biologic and morphologic aspects. Also a chronological summary of B. brasiliensis reports is given. Key words: Taxonomy, Babesia, Babesia brasiliensis, Theileria brasiliensis, Synonym. COMENTARIO TAXONÓMICO baciliformes, arredondadas ou um pouco irregulares, e sem pigmentação malárica, entre O gênero Nuttallia, tal como a maioria dos outras caracte-rísticas. Posteriormente4 o agente protozoologistas conhece1, foi proposto para um foi classificado como Theileria brasiliensis, parasito intraeritrocitário, a Nuttallia herpestedis, apesar de não se relatar o encontro de formas de tendo sido também incluídas no mesmo gênero a multiplicação em linfócitos ou em órgãos N. equi (= Babesia equi ou Theileria equi), e a internos, entre outras características. Nuttallia sp. (= Theileria aristotelis2), parasitos Em uma extensa revisão da classificação dos que apresentavam como características morfo- piroplasmas5 foi proposta a sinonímia do gênero lógicas formato ovalar ou piriforme, com formas Nuttallia assim como de diversos outros gêneros, de multiplicação em cruz (cruz-de-malta) e entre os quais Achromaticus, em relação ao passando por estágios baciliformes.