A core of functionally complementary bacteria colonizes oysters in Pacific Oyster Mortality Syndrome

• Main Authors: Lucasson, Aude, Luo, Xing, Mortaza, Shogofa, de Lorgeril, Julien, Toulza, Eve, Petton, Bruno, Escoubas, Jean-Michel, Clerissi, Camille, Dégremont, Lionel, Gueguen, Yannick, Destoumieux-Garzon, Delphine, Jacq, Annick, Mitta, Guillaume
• Other Authors: Interactions Hôtes-Pathogènes-Environnements (IHPE), Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), Institut de Biologie Intégrative de la Cellule (I2BC), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), Centre de recherches insulaires et observatoire de l'environnement (CRIOBE), Université de Perpignan Via Domitia (UPVD)-École Pratique des Hautes Études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre National de la Recherche Scientifique (CNRS), Unité Santé, Génétique et Microbiologie des Mollusques (SGMM), ANR-10-LABX-0004,CeMEB,Mediterranean Center for Environment and Biodiversity(2010), ANR-14-CE19-0023,DECIPHER,Déchiffrage des maladies multifactorielles: cas des mortalités de l'huître(2014), ANR-19-CE20-0004,DECICOMP,Déchiffrer toute la complexité du syndrome de mortalité des huîtres du Pacifique pour modéliser le risque épidémiologique.(2019), ANR-10-LABX-0041,TULIP,Towards a Unified theory of biotic Interactions: the roLe of environmental(2010)
• Format: Report
• Language: English
• Published: HAL CCSD 2020
• Subjects: [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]; Crassostrea gigas; Pacific oyster
• Online Access: https://hal.science/hal-03054359; https://hal.science/hal-03054359/document; https://hal.science/hal-03054359/file/Lucasson-2020-Biorxiv-Core.pdf; https://doi.org/10.1101/2020.11.16.384644

The Pacific oyster Crassostrea gigas is one of the main cultivated invertebrate species around the world. Since 2008, oyster juveniles have been confronted with a lethal syndrome, Pacific Oyster Mortality Syndrome (POMS). The etiology of POMS is complex. Recently, we demonstrated that POMS is a polymicrobial disease. It is initiated by a primary infection with the herpesvirus OsHV-1 µ Var, and evolves towards a secondary fatal bacteremia that is enabled by the oyster's immunocompromised state. In the present article, we describe the implementation of an unprecedented combination of metabarcoding and metatranscriptomic approaches to show that the sequence of events in POMS pathogenesis is conserved across infectious environments and susceptible oyster genetic backgrounds. We also identify a core colonizing bacterial consortium which, together with OsHV-1 µ Var, forms the POMS pathobiota. This bacterial core is characterized by highly active global metabolism and key adaptive responses to the within-host environment (e.g. stress responses and redox homeostasis). Several marine gamma proteobacteria in the core express different and complementary functions to exploit the host's resources. Such cross-benefits are observed in colonization-related functions, and reveal specific strategies used by these bacteria to adapt and colonize oysters (e.g. adhesion, cell defense, cell motility, metal homeostasis, natural competence, quorum sensing, transport, and virulence). Interdependence and cooperation within the microbial community for metabolic requirements is best exemplified by sulfur metabolism, which is a property of the pathobiota as a whole and not of a single genus. We argue that this interdependence may dictate the conservation of the POMS pathobiota across distinct environments and oyster genetic backgrounds.