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Phylogénie De L'édition Des ARN De Transfert Mitochondriaux Chez Les Université de Montréal Phylogénie de l'édition des ARN de transfert mitochondriaux chez les chytridiomycètes Marie-Josée Laforest Département de biochimie Faculté de médecine Thèse présentée a la Faculté de études supérieures en vue de l'obtention du grade de Philosophiae doctor (PhD.) en Biochimie Juin 2001 O Marie-Josée Laforest, 2001 National Libraq Bibliothèque nationale 1+1 of,mda du Canada Acquisitions and Acquisitions et Bibliographie Services services bibliographiques 395 WeUington Street 395. me Wellinm Ottawa ON KIA ON4 Ottawa ON K1A ON4 Canada Canada The author has granted a non- L'auteur a accordé une licence non exclusive licence allowing the exclusive permettant à la National Library of Canada to Bibliothéque nationale du Canada de reproduce, Ioan, disîriibute or sell reproduire, prêter, distribuer ou copies of this thesis in microform, vendre des copies de cette thèse sous paper or electronic formats. Ia fonne de microfiche/fïlm, de reproduction sur papier ou sur format électronique. The author retains ownership of the L'auteur conserve la propriété du copyright in this thesis. Neither the droit d'auteur qui protège cette thèse. thesis nor substantial extracts fiom it Ni la thèse ni des extraits substantiels may be printed or otherwise de celle-ci ne doivent être imprimés reproduced without the author's ou autrement reproduits sans son ?ermission. autorisation. Université de Montréal Faculté de études supérieures Cette thèse intitulée: Phylogénie de l'édition des ARN de transfert rnitochondriaux chez les chytridiomycètes présentée par : Marie-Josée Laforest a été évaluée par un jury composé des personnes suivantes: Président-rapporteur: Scephen Michnick Directeur de recherche: Franz Lang Membre du jury: Léa Brakier-Gingras Examinateur externe: Gregory Brown thèse acceptée le: Sommaire Les recherches qui ont mené à cette thèse de doctorat ont pour sujet principal l'origine évolutive de I'édition des ARN de transfert (ARNt) présente dans les mitochondries du chytridiom ycète Spizellomyces punctafus et du protiste Acanfhamoeba castellanii. L'édition des ARN réfère à une catégorie de mécanismes qui changent les séquences des ARN par des insertions ou modifications de nucléotides spécifiques, ce qui permet de synthétiser plusieurs protéines a partir d'un gène ou d'améliorer la conservation de la séquence du transcrit. Chez S. punctatus et A. castellanii, la plupart des ARNt codés par leurs génomes mitochondriauxsont édités par un mécanisme qui remplace des nudéotides mésappariésaux trois premières positions des extrémités 5', par des nucléotides qui forment des paires de bases A-U et G-C. Ce mécanisme d'édition restaure la structure conventionnelle des ARNt et, en principe, est essentiel à fa formation dlARNt fonctionels. La découverte de I'édition des ARNt chez ces organismes, qui ne sont pas relies phylogénétiquement, suggérait soit un transfert latéral du ou des gènes codant pour les composantes de l'activité d'édition, soit une évolution indépendante et convergente de mécanismes d'édition des ARNt en apparence similaires. Afin de mieux comprendre l'origine évolutive de ce mécanisme d'édition des ARNt, j'ai développé ce projet de recherche dont le but principal consistait à déterminer la distribution phylogénétiquede I'édition chez les chyttidiomycètes, un groupe de champignons primitifs très diversifiés et peu étudiés. Le premier article présenté dans cette thèse rapporte les résulats du séquençage des ADNmt de quatres espèces de chytridiornycètes, soit Harpochytriumsp. #94, Harpochytn'um #i05, Monoblepharella sp. #15 (Monobléphandales)et Rhizophydiumsp. #A36 (Chytridiales). Comme chez S. punctatus, les ADNmt de ces 4 espèces codent pour des répertoires dJARNt réduits, avec seulement 7 a 9 gènes. L'analyse de ces gènes d'ARNt a révélé que I'édition est présente chez les Monobléphandales, mais est absente chez Rhkophydium sp.. Le séquençage des ARNt, selon un protocole de RT-PCR dlARNt circularisés, a confirmé la présence de l'édition chez les Monobléphandales. Ces résultats ont aussi montré quelques particularités de I'édition des Monobléphandales, incluant des ARNt matures non-édités et I'édition partielle de I'ARNtMM,qui ne sont pas présentes chez S. punctafus. L'analyse phylogénétiquedes protéines rnitochondriales Cob, Coxl ,Cox2, (20x3, Atp6 et Atp9, regroupées en un seul alignement a permis de déduire la phylogénie des chytridiomycètes. Cette phylogénie moléculaire montre que les chytridiomycètesconstituent un groupe paraphylétiquedivisé en trois lignées distinctes: 1) les Blastocladiales (Allomyces macrogynus), 2) les Monoblepharidales et 3) les Spizellomycétales-Chytridiales.Ces deux dernières lignées constituent un clade qui diverge très tbt dans la lignée des champignons, alors que les Blastocladiales divergent à la base des "champignons supérieurs". Selon cette phylogénie mitochondriale, les gènes d'ARNt ont été éliminés avant la divergence des Monobiépharidales, Spizellomycétales et Chytridiales, alors que les Blastocladiales et les "champignons supérieurs" possèdent des répertoires de gènes d'ARNt complets. De plus, nous avons découvert que Rhizophydium sp. utilise le code génétique modifié (UAG pour leucine), comme Spizellomyces. II s'agit d'un caractère dérivé qui est apparu chez un ancêtre des Spizellomycétales et des Chytridiales, alors que les Monoblépharidales et les Blastocladiales ont préservé le code génétique standard, un caractère ancestral des mitochondries. Finalement, cette phylogénie montre que l'édition est présente chez deux lignées distinctes, celles de S. punctatus et des Monoblépharidales, alors qu'elle est absente chez le Chytridiales et les autres champignons. Au cours de ce projet, l'analyse de la séquence de I'ADNmt de S. punctatus a aussi suggéré que le transcrit de son gene cob devait être édité, par des insertion de nucléotides, afin de corriger le cadre de lecture conservé. Le séquençage de ce transcrit par RT-PCR a démontré qu'il n'était pas édité, alors qu'un intron de groupe I de 144 nucléotides, le second intron du gène cob de S. punctatus (Spcob-2), n'avait pas été détecté lors de t'analyse de séquence. De plus, le séquençage du transcrit du gene ml de Rhizophydiurn sp. a aussi permis de confirmer l'absence d'éditior! et la présence d'un intron miniature dans le gene rnl de Rhizophydium sp. (Rdml-S), similaire à Spcob-2. Donc, le second article présenté dans cette thèse rapporte la découverte fortuite d'un nouveau type d'introns de groupe I extrêmement divergents, qui ont moins de 200 nucléotides. Cet article discute principalement des caractéristiques structurales des introns Spcob-2 et Rdml-5, les introns de groupe 1 les plus petits connus jusqu'à maintenant, avec 144 et 142 nucléotides. Cet article rapporte aussi les structures de trois autres introns similaires; Spnad3-1, Rdcoxl-8 et Rdcob-5 avec 164, 180 et 189 nucléotides. Ces introns de groupe I miniatures ont des structures périphériques réduites (ou absentes) et ne possèdent pas les interaction périphériques conservées chez les introns du sous-groupe IB. Par contre, Spcob-2, Rdml-5, Spnad3-1 et Rdcoxl-8 ont des interactions d'appariement potentiels (Pl7*), entre leurs boucles L5 et leurs exons en aval, qui pourraient compenser certains problèmes structuraux de ces introns. De plus, les expériences d'épissage in vitro ont permis de déterminer que les trois introns les plus petits n'ont pas d'activité autocatalytique détectable. Les nombreuses particularités structurales des petits introns Spcob-2 et Rdml-5 montrent qu'il s'agit d'introns extrêmement divergents, ayant évolué à partir d'introns de groupe I canoniques. En conclusion, la distribution phylogénétiquede ce type d'édition des ARNt dans trois lignées mitochondriales distinctes peut ëtre expliquée par une évolution convergente de mécanismes d'édition similaires. Selon les informations actuelles, cette édition des ARNt est apparue au moins trois fois au cours de l'évolution des mitochondries; deux fois chez les chytridiomycètes et une fois dans la lignée de A. castellanii. L'exploration des génomes rnitochondnaux d'autres protistes et champignons, ainsi que la caractérisation des enzymes responsables de ce type d'édition seront nécessaire afin de tester cette hypothèse. Table des matières Sommaire ............................................................ iii Tabledesmatières ..................................................... vi Listedesfigures ....................................................... x Liste des tableaux ...................................................... xii Sigles et abréviations .................................................. xiii Siglesdesacidesarninés ............................................... xvii Dédicace ........................................................... xviii Préface .............................................................. xx Chapitre 1: Introduction ................................................. 1 I. L'évolution moléculaire des mitochondries ............................ 2 1 . 1. Introduction ............................................ 2 1 . 1. 1. Qu'est-ce que la mitochondrie? ..................... 2 1 . 2 . 1. L'origine évolutive de la mitochondrie ................ 3 1.2. La phylogénie moléculaire ................................ 5 1. 2 . 1. Principes de la phylogenie moléculaire .-............. 5 1.2.2. Les méthodes phylogénétiques .................... 6 1. 2 . 3 . Les limitations des phylogénies moléculaires .......... 8 1 . 2 . 4 . Phylogénies moléculaires mitochondriales ...........
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