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The Bacterial Symbiont in the Shallow Water Lucinids Codakia Orbicularis and C

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The Bacterial Symbiont in the Shallow Water Lucinids Codakia Orbicularis and C THÈSE Présentée devant Université Pierre et Marie CURIE Pour l'obtention du Diplôme de DOCTORAT Par Sten König The bacterial symbiont in the shallow water lucinids Codakia orbicularis and C. orbiculata analyzed by physiological proteogenomics directeur: Prof. Hervé Le Guyader (Université Pierre-et-Marie-Curie (UPMC)) co-directeur: Prof. Dr. Olivier Gros (Université Antilles Guyane/UPMC) Prof. Dr. Thomas Schweder (University of Greifswald, Institute of Pharmacy) rapporteur: Prof. Dr. Horst Felbeck (University of California, Scripps Institution of Oceanography) Prof. Dr. Katharina Riedel (University of Greifswald, Institute of Microbiology) Date de soutenance: 17. 12. 2014 i Résumé: Les bivalves côtiers Codakia orbicularis et C. orbiculata, de la famille des Lucinidae, abritent des Gammaprotéobactéries endosymbiotiques sulfo-oxydantes dans leurs branchies. Ces deux bivalves vivent dans les herbiers à Thalassia testudinum et hébergent la même bactérie symbiotique selon les analyses effectuées à partir des séquences d’ADNr 16S. Lors de période de stabulation, la population bactérienne symbiotique décroit alors qu’il n’y a pas, dans le même temps, de relargage des symbiotes observé. Des analyses en cytochimie ont montré une forte activité d’enzymes lysosomales lors de ces épisodes de privation de nourriture et de soufre. Il a ainsi été montré que les symbiotes peuvent servir directement de source de nourriture aux bivalves pour survivre lors de ces périodes de crise. Le transfert de carbone des symbiotes vers l’hôte peut être flexible et pourrait consister en un simple transfert de matière organique ou "milking", dans des conditions normales de nutrition et de digestion des symbiotes et devenir du "farming", dans des conditions de stabulation. Jusqu’à ce jour, le symbiote reste non cultivable. De ce fait, l’utilisation de techniques indépendantes de la culture comme les approches –omics ont été mises en place pour étudier la physiologie de cette bactérie symbiotique. Le génome du symbiote a été analysé par Next Generation Sequencing (NGS) permettant ainsi d’obtenir les bases du protéome et ainsi de pouvoir analyser la physiologie du symbiote. Dans ce travail, le protéome des bactéries a été analysé sous différentes conditions. L’oxydation des sulfures est une des voies métaboliques clés du symbiote de Codakia. Cette voie fait très probablement appel au système Sox périplasmique, ainsi qu’à une sulfite réductase cytoplasmique (DsrAB), une APS réductase (AprAB) et une ATP sulfurylase (SopT). De plus, deux autres enzymes additionnelles d’oxydation des sulfures ont pu être mises en évidence dans l’espace périplasmique du symbiote telle que la quinone réductase (Sqr) et la sulfide déhydrogénase (FccAB). Les gènes des enzymes du cycle de Calvin Benson Bassham (CBB) ne semblent pas être tous présents dans le génome du symbiote. Les protéines de la RuBisCO sont abondamment exprimées. Il semblerait que la régénération du ribulose-1,5-bisphosphate soit effectuée de façon non conventionnelle via une phosphofructokinase PPi-dépendante. Une autre caractéristique du CBB est qu’il y a deux formes différentes de RuBisCO codées dans le génome du symbiote. Les deux formes sont exprimées en même temps, mais la forme I de la RuBisCO est 50 fois plus exprimée que la forme II. En plus de la vie autotrophique, plusieurs gènes nécessaires à une vie hétérotrophique sont présents dans le génome. Dans le protéome, les enzymes de la glycolyse et du cycle TCA sont faiblement exprimées. Les protéines du métabolisme du glycogène ont également été identifiées dans le protéome. De plus, plusieurs types de transporteurs comme ABC, TRAP et PTS sont présents dans le génome et certaines formes d’expression de ces transporteurs ont pu être suspectées, y compris lors de la vie intracellulaire du symbiote. De façon inattendue, un groupe de gènes nif est présent dans le génome permettant la fixation de l’azote atmosphérique par le symbiote. Les protéines codées par les gènes clés, comme la nitrogénase NifH/K/D, ont été abondamment trouvées dans le ii protéome. De plus, l’analyse du protéome montre une régulation forte de ces protéines dans des conditions de stabulation du bivalve hôte. La rubrerythrine est fortement exprimée et servirait à protéger la nitrogénase de l’oxygène au sein des bacteriocytes. L’endosymbiote bactérien code également pour un système de sécrétion de type 6 (T6SS) pour le transport de molécules bactériennes effectrices à travers les membranes du cytoplasme de la cellule hôte et jouerait un rôle possible de communication directe avec l’hôte. En résumé, les analyses génomiques et protéomiques du symbiote bactérien des Codakia améliorent notre connaissance des voies métaboliques majeures des bivalves Lucinidae. L’ensemble des données de cette étude pourra servir à de futures analyses plus poussées de la physiologie et des interactions métaboliques entre l’hôte et ses symbiotes. mot-clé: symbiose, Codakia orbicularis, Codakia orbiculata, soufre metabolisme, proteomics, genomics key words: symbiosis, Codakia orbicularis, Codakia orbiculata, sulfur metabolism, proteomics, genomics iii This PhD thesis includes results of a paper this was accepted 10. November. 2014 in the journal Microscopy Research and Technique. Thioautotrophic bacterial endosymbionts are degraded by enzymatic digestion during starvation: case study of two lucinids - Codakia orbicularis and C. orbiculata. Sten König1, Hervé Le Guyader2 and Olivier Gros1,3 1 Institut de Biologie Paris-Seine, UMR 7138 - Evolution Paris-Seine, Equipe Biologie de la Mangrove. Université des Antilles et de la Guyane, UFR des Sciences Exactes et Naturelles, Département de Biologie, BP 592. 97159 Pointe-à-Pitre cedex, Guadeloupe, France. 2 Sorbonne Universités Paris VI, Institut de Biologie Paris-Seine, UMR 7138 - Evolution Paris-Seine, Equipe Phylogénie, Anatomie, Evolution. C.N.R.S, Institut de Biologie Paris-Seine, UMR 7138 - Evolution Paris-Seine, Equipe Biologie de la Mangrove. 3 C3MAG, UFR des Sciences Exactes et Naturelles, Université des Antilles et de la Guyane, BP 592 - 97159 Pointe-à-Pitre, Guadeloupe, French West Indies. iv Table of contents 1. Introduction ....................................................................................................... 1 1.1 An overview of symbiosis ................................................................................... 1 1.1.1 Marine chemosynthesis ..................................................................................................... 3 1.2 Chemoautotrophic symbiosis ............................................................................. 4 1.3 Codakia orbicularis and C. orbiculata and its chemoautotrophic symbiont ... 6 1.4 Ecosystem Thalassia testudinum - habitat of Codakia ....................................12 1.5 Objectives - aim of this thesis ............................................................................13 2. Material and Methods ...................................................................................... 14 2.1 Material ................................................................................................................14 2.1.1 Software and databases .................................................................................................. 14 2.1.2 Chemicals ........................................................................................................................ 14 2.2 Methods ...............................................................................................................14 2.2.1 Sampling of bivalves ........................................................................................................ 14 2.2.2 Bivalve incubation - Induction of symbiont's loss............................................................. 15 2.2.3 Cytochemistry - arylsulfatase and acid phosphatase detection ...................................... 15 2.2.4 Purification of the bacterial fraction - density centrifugation ............................................ 16 2.2.5 Sequencing of the Codakia symbionts ............................................................................ 17 2.2.6 Gene annotation .............................................................................................................. 17 2.2.7 Database creation for proteomics .................................................................................... 18 2.2.8 Metabolic Pathways ......................................................................................................... 18 2.2.9 Proteomics ....................................................................................................................... 18 2.2.9.1 Extraction of soluble proteins .................................................................................. 18 2.2.9.2 Enrichment of the membrane proteins .................................................................... 18 2.2.9.3 1D gel SDS PAGE .................................................................................................. 19 2.2.9.4 In-gel protein digestion and ESI MS/MS analyses .................................................. 20 2.2.9.5 Protein identification and data analysis with Scaffold ............................................. 20 2.2.9.6 2D SDS PAGE ........................................................................................................ 21 2.2.9.7 2D gel protein spot digestion and identification with MALDI-ToF ........................... 21 2.2.9.8 Gel free proteomics - Synapt G2 ...........................................................................
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