A core of functional complementary bacteria infects oysters in Pacific Oyster Mortality Syndrome

Abstract

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.

Seaweeds influence oyster microbiota and disease susceptibility

“…Tissue damage from infections can promote colonization by a wide variety of opportunistic bacteria from the surrounding environment. This is what happens during OsHV‐1 infection (see de Lorgeril et al, 2018; Lucasson et al, 2020 and this study), and in other diseases affecting corals (Closek et al, 2014; Roder et al, 2014). The shift in the relative abundance of Mollicutes at the benefit of Alphaproteobacteria has never been reported before.…”

“…Dysbiosis leads to a secondary colonization by opportunistic bacterial pathogens and oyster death. The reshuffling of the oyster microbiota is an integral part of the infectious process induced by OsHV‐1 (Lucasson et al, 2020). In addition, oysters with differing levels of resistance to POMS exhibit constitutive differences in their bacterial microbiota, suggesting that it might play a role in host immunity (Clerissi et al, 2020; King et al, 2019; Pathirana et al, 2019).…”

The Pacific Oyster Mortality Syndrome, a Polymicrobial and Multifactorial Disease: State of Knowledge and Future Directions

“…Recently, we studied the structure of bacterial communities (as determined by 16S metabarcoding) and the functions expressed by different bacterial genera (as determined by metatranscriptomics) in different oyster biparental families submitted to different infectious environment ( 55 ). Five bacterial genera ( Arcobacter, Marinobacterium, Marinomonas, Vibrio , and Pseudoalteromonas) that colonize oysters during POMS were remarkably consistent between families and environments.…”

“…The core functions identified by metatranscriptomics in POMS pathobiota reveal the importance of general metabolism and adaptation to stress (imposed by host defenses) in the success of colonization ( 55 ). Beyond general metabolism, detoxifying enzymes (such as alkylhydroxyperoxydases) involved in the resistance to or tolerance of host immune defenses are expressed by all successful colonizers.…”

“…A number of genus-specific functions that likely confer cross-benefits at the community level are also expressed during pathogenesis ( 55 ). These include genes related to metal homeostasis (siderophore production), iron uptake, and virulence ( e.g.…”