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.

Background The Pacific oyster Crassostrea gigas is one of the main cultivated invertebrate species worldwide. Since 2008, oyster juveniles have been confronted with a lethal syndrome known as the Pacific Oyster Mortality Syndrome (POMS). POMS is a polymicrobial disease initiated by a primary infection with the herpesvirus OsHV-1 µVar that creates an oyster immunocompromised state and evolves towards a secondary fatal bacteremia. Results 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. We also identified a core bacterial consortium which, together with OsHV-1 µVar, forms the POMS pathobiota. This bacterial consortium is characterized by high transcriptional activities and complementary metabolic functions to exploit host’s resources. A significant metabolic specificity was highlighted at the bacterial genus level, suggesting low competition for nutrients between members of the core bacteria. Conclusions Lack of metabolic competition between the core bacteria might favor complementary colonization of host tissues and contribute to the conservation of the POMS pathobiota across distinct infectious environments.