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

Abstract

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.

Cross-talk and mutual shaping between the immune system and the microbiota during an oyster's life

“…Answering such an essential question requires a deeper understanding of microbial community gene functions, beyond descriptions of their taxonomic composition. Although recent progress has been made in this direction [ 11 , 26 , 136 ], it is not clear yet whether oyster microbiota is shaped according to microbial community gene function and regulation, particularly in a healthy context. To address this challenging question, several difficulties have to be circumvented.…”

“…Sequentially, the infection by OsHV-1 µVar triggers an immune-compromised state that induces microbiota dysbiosis and subsequent bacteraemia, ultimately leading to oyster death. Fatal dysbiosis is accompanied by invasion of the connective tissue by opportunistic bacteria and in particular Vibrio and Arcobacter , which are consistently associated with oyster death [ 26 ]. The virus alters antibacterial defences by infecting haemocytes and reprogramming their functions.…”

“…OsHV-1 µVar alters more particularly AMP expression, which coincides with a loss of control of microbial communities 24 h after viral infection [ 23 ]. The sequence of events leading to dysbiosis and oyster death is conserved across infectious environments in France (Mediterreanean, Atlantic) and oyster genetic backgrounds [ 26 ]. Moreover, using a combination of amplicon sequencing and metatranscriptomics, a core pathobiota assemblage was identified; it colonizes oysters during the secondary bacterial infection of oysters in POMS.…”

“…It may also be attributed to limited competition for resources among these genera, implying an efficient utilization of the diverse resources in the oyster environment, supporting the robust growth of bacteria with distinct metabolic characteristics. This functional complementarity may explain the taxonomic conservation of the POMS pathobiota [ 26 ].…”

“…A fine-tuned dialogue between oyster immunity and its microbiota was evidenced from early life to adult stages [ 23 – 25 ]. Recently a first insight into microbial community gene functions has been made accessible, either by shotgun metagenomics [ 11 ] or metatranscriptomics [ 26 ]. The present article summarizes the knowledge accumulated on oyster–microbiota interactions over the last few years and reviews the dysregulations leading to dysbiosis and oyster death.…”