Inefficient immune response is associated with microbial permissiveness in juvenile oysters affected by mass mortalities on field

Type Article
Date 2018-06
Language English
Author(s) de Lorgeril JulienORCID1, Escoubas Jean Michel1, Loubiere Vincent1, 6, Pernet FabriceORCID2, Le Gall Patrik3, Vergnes Agnes1, Aujoulat Fabien4, Jeannot Jean-Luc4, Jumas-Bilak Estelle4, Got Patrice5, Gueguen YannickORCID1, Destoumieux-Garzon DelphineORCID1, Bachere Evelyne1
Affiliation(s) 1 : Univ Perpignan, Univ Montpellier, IHPE, CNRS,Ifremer, Via Domitia, Perpignan, France.
2 : Ifremer, LEMAR UMR6539, CNRS UBO IRD Ifremer, F-29280 Plouzane, France.
3 : CNRS IRD Ifremer UM, MARBEC UMR 9190, F-34203 Sete, France.
4 : Univ Montpellier, CNRS, IRD, UMR HydroSci Montpellier 5569,Equipe Pathogens Hy, Montpellier, France.
5 : CNRS IRD Ifremer UM, MARBEC UMR 9190, F-34095 Montpellier, France.
6 : Univ Montpellier, CNRS, UMR 9002, Inst Human Genet, Montpellier, France.
Source Fish & Shellfish Immunology (1050-4648) (Academic Press Ltd- Elsevier Science Ltd), 2018-06 , Vol. 77 , P. 156-163
DOI 10.1016/j.fsi.2018.03.027
WOS© Times Cited 16
Keyword(s) Host pathogen interaction, Innate immunity, Invertebrate, Mollusk, In situ mortality, Total bacteria, Crassostrea gigas

Since 2008, juvenile Crassostrea gigas oysters have suffered from massive mortalities in European farming areas. This disease of complex etiology is still incompletely understood. Triggered by an elevated seawater temperature, it has been associated to infections by a herpes virus named OsHV-1 as well as pathogenic vibrios of the Splendidus clade. Ruling out the complexity of the disease, most of our current knowledge has been acquired in controlled experiments. Among the many unsolved questions, it is still ignored what role immunity plays in the capacity oysters have to survive an infectious episode. Here we show that juvenile oysters susceptible to the disease mount an inefficient immune response associated with microbial permissiveness and death. We found that, in contrast to resistant adult oysters having survived an earlier episode of mortality, susceptible juvenile oysters never exposed to infectious episodes died by more than 90% in a field experiment. Susceptible oysters were heavily colonized by OsHV-1 herpes virus as well as bacteria including vibrios potentially pathogenic for oysters, which proliferated in oyster flesh and body fluids during the mortality event. Nonetheless, susceptible oysters were found to sense microbes as indicated by an overexpression of immune receptors and immune signaling pathways. However, they did not express important immune effectors involved in antimicrobial immunity and apoptosis and showed repressed expression of genes involved in ROS and metal homeostasis. This contrasted with resistant oysters, which expressed those important effectors, controlled bacterial and viral colonization and showed 100% survival to the mortality event. Altogether, our results demonstrate that the immune response mounted by susceptible oysters lacks some important immune functions and fails in controlling microbial proliferation. This study opens the way to more holistic studies on the “mass mortality syndrome”, which are now required to decipher the sequence of events leading to oyster mortalities and determine the relative weight of pathogens, oyster genetics and oyster-associated microbiota in the disease.

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de Lorgeril Julien, Escoubas Jean Michel, Loubiere Vincent, Pernet Fabrice, Le Gall Patrik, Vergnes Agnes, Aujoulat Fabien, Jeannot Jean-Luc, Jumas-Bilak Estelle, Got Patrice, Gueguen Yannick, Destoumieux-Garzon Delphine, Bachere Evelyne (2018). Inefficient immune response is associated with microbial permissiveness in juvenile oysters affected by mass mortalities on field. Fish & Shellfish Immunology, 77, 156-163. Publisher's official version : , Open Access version :