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Viruses of Hyperthermophilic Archaea: Entry and Egress from the Host Cell

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Viruses of hyperthermophilic archaea : entry and egress from the host cell Emmanuelle Quemin To cite this version: Emmanuelle Quemin. Viruses of hyperthermophilic archaea : entry and egress from the host cell. Microbiology and Parasitology. Université Pierre et Marie Curie - Paris VI, 2015. English. NNT : 2015PA066329. tel-01374196 HAL Id: tel-01374196 https://tel.archives-ouvertes.fr/tel-01374196 Submitted on 30 Sep 2016 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Université Pierre et Marie Curie – Paris VI Unité de Biologie Moléculaire du Gène chez les Extrêmophiles Ecole doctorale Complexité du Vivant ED515 Département de Microbiologie - Institut Pasteur 7, quai Saint-Bernard, case 32 25, rue du Dr. Roux 75252 Paris Cedex 05 75015 Paris THESE DE DOCTORAT DE L’UNIVERSITE PIERRE ET MARIE CURIE Spécialité : Microbiologie Pour obtenir le grade de DOCTEUR DE L’UNIVERSITE PIERRE ET MARIE CURIE VIRUSES OF HYPERTHERMOPHILIC ARCHAEA: ENTRY INTO AND EGRESS FROM THE HOST CELL Présentée par M. Emmanuelle Quemin Soutenue le 28 Septembre 2015 devant le jury composé de : Prof. Guennadi Sezonov Président du jury Prof. Christa Schleper Rapporteur de thèse Dr. Paulo Tavares Rapporteur de thèse Dr. Claire Geslin Examinateur Dr. Jacomine Krijnse-Locker Examinateur Dr. David Prangishvili Directeur de thèse Dr. Mart Krupovic Superviseur de thèse VIRUSES OF HYPERTHERMOPHILIC ARCHAEA: ENTRY INTO AND EGRESS FROM THE HOST CELL A mes parents, A ma grand-mère, Viruses Of Hyperthermophilic Archaea: Entry Into And Egress From The Host Cell RESUME ........................................................................................................................................................... 1 ABSTRACT ........................................................................................................................................................ 3 Key words ........................................................................................................................................................... 3 INTRODUCTION ................................................................................................................................................ 9 The third domain of life. ..................................................................................................................................... 9 Highly diversified archaea. ................................................................................................................................ 11 Unique archaeal virosphere. ............................................................................................................................. 12 Sulfolobus, a model for hyperthermophilic archaea. ....................................................................................... 17 Cell surface characteristics. .............................................................................................................................. 18 Cell surface appendages. .................................................................................................................................. 19 Insights into the biology of hyperthermophilic archaeal viruses. ..................................................................... 22 SSV1. ................................................................................................................................................................. 23 SIRV2. ................................................................................................................................................................ 24 Virus-host interactions in Archaea: state-of-the-art. ....................................................................................... 25 CHAPTER 1 ..................................................................................................................................................... 31 Insights into the biology of archaeal viruses by high-throughput approaches................................................. 31 CHAPTER 2 ..................................................................................................................................................... 37 Virus-host interactions in Archaea - the best is yet to come. ........................................................................... 37 CHAPTER 3 ..................................................................................................................................................... 49 Unique spindle-shaped viruses in Archaea. ...................................................................................................... 49 CHAPTER 4 ..................................................................................................................................................... 57 One update on the architecture of SSV1 virions. ............................................................................................. 57 CHAPTER 5 ..................................................................................................................................................... 85 The egress of SSV1 or how to bud from an archaeon. ..................................................................................... 85 CHAPTER 6 ................................................................................................................................................... 107 Unravelling the early stages of SIRV2 infection. ............................................................................................. 107 DISCUSSION ................................................................................................................................................. 119 Successful spindle-shaped archaeal viruses. .................................................................................................. 119 Architecture of spindle-shaped virions: the case-study of SSV1. ................................................................... 120 SSV1 as a model for lipid-containing viruses infecting archaea...................................................................... 121 SIRV2 as a model for non-enveloped viruses infecting archaea. .................................................................... 127 Concluding remarks and future perspectives. ................................................................................................ 130 REFERENCES ................................................................................................................................................. 133 ACKNOWLEDGMENTS .................................................................................................................................. 145 MEMBERS OF THE JURY................................................................................................................................ 147 RESUME Les archées sont principalement connues pour leur capacité à croître et survivre dans des conditions extrêmes de température, pression, pH, etc. qui sont hostiles à l’homme. Néanmoins, il est désormais clair que les archées sont aussi présentes de manière ubiquitaire dans divers environnements. L’étude détaillée des différents aspects de la biologie de ces microorganismes a amené à des découvertes pour le moins inattendues comme celle de la virosphère associée aux archées qui est unique. En effet, plusieurs virus infectant les archées ont été isolés et présentent une incroyable diversité tant au niveau morphologique que génomique et ne ressemblent aucunement aux virus connus de bactéries ou d’eucaryotes. Récemment, l’analyse en détails du cycle viral a mis à jour de nouveaux mécanismes d’interactions avec la cellule hôte. Au cours de mes travaux de thèse, nous nous sommes intéressés aux systèmes virus-hôtes présents dans les milieux hyperthermiques et acidophiles en sélectionnant les virus fusiforme et filamenteux SSV1 et SIRV2 en tant que modèles d’étude. Tout d’abord, nous avons défini une nouvelle classification des virus fusiformes basée sur l’analyse comparative des protéines structurales et des génomes viraux. L’ensemble des virus considérés forme un réseau global malgré le fait qu’ils ont été isolés dans des environnements distincts ; qu’ils infectent des hôtes qui sont distant phylogénétiquement parlant et que certains de leurs virions présentent une certaine pléomorphicité. Ensuite, la caractérisation en détails de l’architecture des virions fusiformes de SSV1 a révélé qu’ils étaient enveloppés, composés de protéines de capside glycosylées et contenaient le complexe nucléoprotéique. Finalement, nous nous sommes concentrés sur la manière dont les virus d’archées interagissent avec la cellule hôte. Alors que les virions de SIRV2 semblent utiliser une stratégie pour l’entrée qui est similaire aux bactériophages dits flagellotrophiques ; on observe que les virions de SSV1 emploient un mécanisme de sortie qui rappelle le bourgeonnement des virus eucaryotes enveloppés. L’ensemble de ces recherches participent à une meilleure compréhension
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