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Comprehensive Study of New Virulent Bacteriophages : from Transcriptomic and Mechanistic Characterisations Towards Evolutionary Perspectives Anne Chevallereau

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Comprehensive Study of New Virulent Bacteriophages : from Transcriptomic and Mechanistic Characterisations Towards Evolutionary Perspectives Anne Chevallereau Comprehensive study of new virulent bacteriophages : from transcriptomic and mechanistic characterisations towards evolutionary perspectives Anne Chevallereau To cite this version: Anne Chevallereau. Comprehensive study of new virulent bacteriophages : from transcriptomic and mechanistic characterisations towards evolutionary perspectives. Microbiology and Parasitology. Uni- versité Sorbonne Paris Cité, 2017. English. NNT : 2017USPCC162. tel-02079406 HAL Id: tel-02079406 https://tel.archives-ouvertes.fr/tel-02079406 Submitted on 26 Mar 2019 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. Thèse de doctorat de l’Université Sorbonne Paris Cité Préparée à l’Université Paris Diderot Ecole doctorale Bio Sorbonne Paris Cité (ED157) Unité de Biologie Moléculaire du Gène chez les Extrêmophiles Groupe Interactions Phages-Bactéries chez l’Animal Institut Pasteur Thèse de doctorat de Microbiologie Par Anne CHEVALLEREAU Comprehensive study of new virulent bacteriophages: From transcriptomic and mechanistic characterisations towards evolutionary perspectives Présentée et soutenue publiquement à Paris le 19 Mai 2017 Pr. Isabelle Martin -Verstraete (Université Paris Diderot) Présidente Dr. Mireille Ansaldi ( CNRS / Université Ai x Marseille) Rapportrice Dr. Darren Smith (University of Northumbria) Rapporteur Pr. Olga Soutourina (Université Paris Sud) Examinatrice Dr. Romé Voulhoux ( CNRS / Université Aix -Marseille) Examinateur Dr. Laurent Derbarbieux (Insitut Pasteur) Directeur de thèse Thèse de doctorat dl’UnivrsitéSorbonnParisCité Préparée ,l’ Université Paris Diderot Ecole doctorale Bio Sorbonne Paris Cité (ED157) Unité de Biologie Moléculaire du Gène chez les Extrêmophiles Groupe Interactions Phages- Bctéris,chz,l’;niml, Institut Pasteur Thèse de doctorat de Microbiologie Par Anne CHEVALLEREAU Comprehensive study of new virulent bacteriophages: From transcriptomic and mechanistic characterisations towards evolutionary perspectives Présentée et soutenue publiquement à Paris le 19 Mai 2017 Pr. Isabelle Martin-Verstraete (Université Paris Diderot) Présidente Dr. Mireille Ansaldi (CNRS / Université Aix Marseille) Rapportrice Dr. Darren Smith (University of Northumbria) Rapporteur Pr. Olga Soutourina (Université Paris Sud) Examinatrice Dr. Romé Voulhoux (CNRS / Université Aix-Marseille) Examinateur Dr. Laurent Derbarbieux (Insitut Pasteur) Directeur de thèse 1 2 Etude globale de deux nouveaux bactériophages virulents : Caractérisations transcriptomique, mécanistique et perspectives évolutives Résumé: Soutenue par le renouveau de la phagothérapie, la découverte de nouveaux bactériophages (phages) nous a permis de définir deux n ouveaux genres de virus dénommés Kpp10virus et Pakpunavirus dont les mécanismes infectieux sont inconnus. Il est admis que l, succès, d’ un cycle infectieux est notamment assuré par une réappropriation efficace des ressources de la cellule hôte, conduisant à sa transformation en « virocellule », c’st -à-dire, un organisme cellulaire exclusivement dédié à la production de particules virales. Ce travail de thèse ,pour,objctif,d’pportr, une vision globale des stratégies moléculaires utilisées par les virus appartenant aux genres Kpp10virus et Pakpunavirus (respectivement représentés par les phages PAK_P3 et PAK_P4) pour infecter le pathogène opportuniste Pseudomonas aeruginosa. Dans un premier temps, nous avons évalué leurs propriétés intrinsèques en analysant le contenu de leurs génoms,lurs,spctrs,d’hôts , leurs paramètres de croissance insi,qu’ en identifiant leur récepteur bactérien. Dns, un, scond, tmps, un, combinison, d’pprochs, trnscriptomiq ues et métabolomiques a permis de montrer que ces deux virus ont des programmes transcriptionnels similaires, incluant notamment une régulation temporelle de leur expression génétique et la production de transcrits antisens. De plus, ils provoquent tous de ux,l,dégrdtion,rpid,d,90%,ds,;RNm,d,l’hôt , qui sont alors remplacés par des ARNm viraux. Malgré cette dégradation, nous avons constaté que ces deux phages redirigent les voies de biosynthèse bactériennes plutôt que de provoquer une extinction totale du métabolisme cellulaire, en utilisant cependant des mécanismes différents. De plus, nous avons détecté l’ctivtion,pr,l’hôt,d’un,répons,commun, suite à une infection par P;K_P3, ou, P;K_P4, t, vons, émis, l’hypothès, qu’il, s’git, d’un, tnttiv, d réparation des importants dommgs,;RN,induits,pr,l’infction,virl Enfin, nous, vons, étudié, ls, fonctions, d’un, protéin, virl (Gp92), largement conservée chez les virus appartenant à ces deux genres et qui est produite au stade précoce du cycle infectieux ,Lorsqu’ll,st,produit, sul,chz,l’hôt,ctt,protéin altère la morphologie cellulaire et interagit avec un complexe de régulation bactérien de type facteur sigma/anti-sigma impliqué dans la réponse au stress (appelé AlgU-MucA). Notre étude suggère un rôle potentiel de Gp92 dns,l’tténution,du,strss,provoqué,pr,l’infction,virl, Ce mnuscrit,fournit,un,modèl,d,trnsformtion,d’un,cllul,d, P. aeruginosa en « virocellule » au cours de l’infction,pr,P;K_P3,ou,P;K_P4, De plus, la comparaison des stratégies de ces deux virus, vraisemblablement issus,d’un,ncêtr,commun nous a permis de discuter l’évolution,ds,mécnisms,infctiux,chz,ls,phgs, virulents. Mots clefs : Kpp10virus , Pakpunavirus, « virocellule », P. aeruginosa, étude transcriptomique. 3 Comprehensive study of new virulent bacteriophages: From transcriptomic and mechanistic characterisations towards evolutionary perspectives Abstract : Previous investigations in the field of phage therapy led to the discovery of two new genera of bacteriophages (phages), namely Kpp10virus and Pakpunavirus whose infection mechanisms are unknown . It is acknowledged that a successful infection is notably ensured by an effective takeover of host cell resources, leading to its transformation into a virocell , a cellular organism exclusively dedicated to the production of progeny phages. This PhD work aims to provide a comprehensive view of molecular strategies set up by Kpp10virus and Pakpunavirus (represented by phages PAK_P3 and PAK_P4, respectively) to infect the opportunist pathogen Pseudomonas aeruginosa . First, we assessed phage intrinsic properties by analyzing their genomic content, evaluating their host range and growth parameters and identifying their bacterial receptor. Then, by coupling transcriptomics and metabolomics approaches, we found that both viruses have similar transcriptional programs, with a temporal regulation of their gene expression and production of antisense transcripts. They both strikingly prompt a rapid degradation of 90% of host mRNAs, which are eventually replaced by viral RNAs. Despite this extensive degradation, we found that both phages do not shutoff host metabolism but redirect biosynthesis pathways, however through different mechanisms. In addition, we found that a common host response is elicited upon both PAK_P3 and PAK_P4 infections and hypothesized it represents an attempt of the host to repair extensive RNA damage. Finally, we investigated the functions of an early produced phage protein (Gp92), broadly conserved in both phage genera, in order to identify particular mechanisms of host subversion used by these phages. When expressed alone in the host, Gp92 alters cell morphology and interacts with the bacterial regulatory complex sigma/anti-sigma involved in stress response (namely AlgU- MucA). Our study suggests a potential role of Gp92 in alleviating the stress caused by phage infection. This manuscript provides a model of virocell transformation upon infection of P. aeruginosa by PAK_P3 or PAK_P4. In addition, by comparing their reproductive strategies, it addresses the evolution of infection mechanisms in virulent phages deriving from a common ancestor. Keywords : Kpp10virus , Pakpunavirus, virocell -conversion , P. aeruginosa, transcriptomic study 4 A Kadoc .:l’aube:de:jours:nouveaux . 5 Acknowledgments / Remerciements First, I would like to thank all the members of the jury for their time and consideration. I thank Isabelle Martin-Verstraete for chairing this committee. Thanks to Mireille Ansaldi and Darren Smith for accepting to review this manuscript and travelling all the way from the very south of France, or from the very north of England. Thanks to Olga Soutourina and Romé Voulhoux for accepting to examine this work. Je tiens à remercier Patrick Forterre, responsable d,l’unité,Biologi,Moléculir,du,Gèn,chz,ls, Extrêmophils,pour,m’voir,prmis,d,rélisr,m,thès,u,sin,d,son,lbortoir J’drss,ms,sincèrs,rmrcimnts,,mon,dirctur,d,thès,Lurnt,Dbrbiux,pour,m’voir, offert la possibilité, tant convoitée, de travailler sur les phages. Entr,l’bsnc,d,plc,disponibl au lbo,t,l’incrtitud,d,pouvoir,prticipr,u,concours,d,l’écol,doctorl,tu,s,qund,mêm,rndu, cl,possibl,t,j,t’n,suis, reconnaissante. Merci également pour ta disponibilité, ton soutien dans l’dvrsité,t, surtout pour ta confiance et la liberté qu,tu,m’s,lissé,,pour,mnr,c,projt I express my deep gratitude to Rob Lavigne who made this project possible in the first place, for welcoming
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