Cargando…

Understanding the Dynamic of POMS Infection and the Role of Microbiota Composition in the Survival of Pacific Oysters, Crassostrea gigas

For over a decade, Pacific oyster mortality syndrome (POMS), a polymicrobial disease, induced recurring episodes of massive mortality affecting Crassostrea gigas oysters worldwide. Recent studies evidenced a combined infection of the ostreid herpesvirus (OsHV-1 μVar) and opportunistic bacteria in af...

Descripción completa

Detalles Bibliográficos
Autores principales: Delisle, Lizenn, Laroche, Olivier, Hilton, Zoë, Burguin, Jean-François, Rolton, Anne, Berry, Jolene, Pochon, Xavier, Boudry, Pierre, Vignier, Julien
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769987/
https://www.ncbi.nlm.nih.gov/pubmed/36314927
http://dx.doi.org/10.1128/spectrum.01959-22
_version_ 1784854493856268288
author Delisle, Lizenn
Laroche, Olivier
Hilton, Zoë
Burguin, Jean-François
Rolton, Anne
Berry, Jolene
Pochon, Xavier
Boudry, Pierre
Vignier, Julien
author_facet Delisle, Lizenn
Laroche, Olivier
Hilton, Zoë
Burguin, Jean-François
Rolton, Anne
Berry, Jolene
Pochon, Xavier
Boudry, Pierre
Vignier, Julien
author_sort Delisle, Lizenn
collection PubMed
description For over a decade, Pacific oyster mortality syndrome (POMS), a polymicrobial disease, induced recurring episodes of massive mortality affecting Crassostrea gigas oysters worldwide. Recent studies evidenced a combined infection of the ostreid herpesvirus (OsHV-1 μVar) and opportunistic bacteria in affected oysters. However, the role of the oyster microbiota in POMS is not fully understood. While some bacteria can protect hosts from infection, even minor changes to the microbial communities may also facilitate infection and worsen disease severity. Using a laboratory-based experimental infection model, we challenged juveniles from 10 biparental oyster families with previously established contrasted genetically based ability to survive POMS in the field. Combining molecular analyses and 16S rRNA gene sequencing with histopathological observations, we described the temporal kinetics of POMS and characterized the changes in microbiota during infection. By associating the microbiota composition with oyster mortality rate, viral load, and viral gene expression, we were able to identify both potentially harmful and beneficial bacterial amplicon sequence variants (ASVs). We also observed a delay in viral infection resulting in a later onset of mortality in oysters compared to previous observations and a lack of evidence of fatal dysbiosis in infected oysters. Overall, these results provide new insights into how the oyster microbiome may influence POMS disease outcomes and open new perspectives on the use of microbiome composition as a complementary screening tool to determine shellfish health and potentially predict oyster vulnerability to POMS. IMPORTANCE For more than a decade, Pacific oyster mortality syndrome (POMS) has severely impacted the Crassostrea gigas aquaculture industry, at times killing up to 100% of young farmed Pacific oysters, a key commercial species that is cultivated globally. These disease outbreaks have caused major financial losses for the oyster aquaculture industry. Selective breeding has improved disease resistance in oysters, but some levels of mortality persist, and additional knowledge of the disease progression and pathogenicity is needed to develop complementary mitigation strategies. In this holistic study, we identified some potentially harmful and beneficial bacteria that can influence the outcome of the disease. These results will contribute to advance disease management and aquaculture practices by improving our understanding of the mechanisms behind genetic resistance to POMS and assisting in predicting oyster vulnerability to POMS.
format Online
Article
Text
id pubmed-9769987
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-97699872022-12-22 Understanding the Dynamic of POMS Infection and the Role of Microbiota Composition in the Survival of Pacific Oysters, Crassostrea gigas Delisle, Lizenn Laroche, Olivier Hilton, Zoë Burguin, Jean-François Rolton, Anne Berry, Jolene Pochon, Xavier Boudry, Pierre Vignier, Julien Microbiol Spectr Research Article For over a decade, Pacific oyster mortality syndrome (POMS), a polymicrobial disease, induced recurring episodes of massive mortality affecting Crassostrea gigas oysters worldwide. Recent studies evidenced a combined infection of the ostreid herpesvirus (OsHV-1 μVar) and opportunistic bacteria in affected oysters. However, the role of the oyster microbiota in POMS is not fully understood. While some bacteria can protect hosts from infection, even minor changes to the microbial communities may also facilitate infection and worsen disease severity. Using a laboratory-based experimental infection model, we challenged juveniles from 10 biparental oyster families with previously established contrasted genetically based ability to survive POMS in the field. Combining molecular analyses and 16S rRNA gene sequencing with histopathological observations, we described the temporal kinetics of POMS and characterized the changes in microbiota during infection. By associating the microbiota composition with oyster mortality rate, viral load, and viral gene expression, we were able to identify both potentially harmful and beneficial bacterial amplicon sequence variants (ASVs). We also observed a delay in viral infection resulting in a later onset of mortality in oysters compared to previous observations and a lack of evidence of fatal dysbiosis in infected oysters. Overall, these results provide new insights into how the oyster microbiome may influence POMS disease outcomes and open new perspectives on the use of microbiome composition as a complementary screening tool to determine shellfish health and potentially predict oyster vulnerability to POMS. IMPORTANCE For more than a decade, Pacific oyster mortality syndrome (POMS) has severely impacted the Crassostrea gigas aquaculture industry, at times killing up to 100% of young farmed Pacific oysters, a key commercial species that is cultivated globally. These disease outbreaks have caused major financial losses for the oyster aquaculture industry. Selective breeding has improved disease resistance in oysters, but some levels of mortality persist, and additional knowledge of the disease progression and pathogenicity is needed to develop complementary mitigation strategies. In this holistic study, we identified some potentially harmful and beneficial bacteria that can influence the outcome of the disease. These results will contribute to advance disease management and aquaculture practices by improving our understanding of the mechanisms behind genetic resistance to POMS and assisting in predicting oyster vulnerability to POMS. American Society for Microbiology 2022-10-31 /pmc/articles/PMC9769987/ /pubmed/36314927 http://dx.doi.org/10.1128/spectrum.01959-22 Text en Copyright © 2022 Delisle et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Delisle, Lizenn
Laroche, Olivier
Hilton, Zoë
Burguin, Jean-François
Rolton, Anne
Berry, Jolene
Pochon, Xavier
Boudry, Pierre
Vignier, Julien
Understanding the Dynamic of POMS Infection and the Role of Microbiota Composition in the Survival of Pacific Oysters, Crassostrea gigas
title Understanding the Dynamic of POMS Infection and the Role of Microbiota Composition in the Survival of Pacific Oysters, Crassostrea gigas
title_full Understanding the Dynamic of POMS Infection and the Role of Microbiota Composition in the Survival of Pacific Oysters, Crassostrea gigas
title_fullStr Understanding the Dynamic of POMS Infection and the Role of Microbiota Composition in the Survival of Pacific Oysters, Crassostrea gigas
title_full_unstemmed Understanding the Dynamic of POMS Infection and the Role of Microbiota Composition in the Survival of Pacific Oysters, Crassostrea gigas
title_short Understanding the Dynamic of POMS Infection and the Role of Microbiota Composition in the Survival of Pacific Oysters, Crassostrea gigas
title_sort understanding the dynamic of poms infection and the role of microbiota composition in the survival of pacific oysters, crassostrea gigas
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769987/
https://www.ncbi.nlm.nih.gov/pubmed/36314927
http://dx.doi.org/10.1128/spectrum.01959-22
work_keys_str_mv AT delislelizenn understandingthedynamicofpomsinfectionandtheroleofmicrobiotacompositioninthesurvivalofpacificoysterscrassostreagigas
AT larocheolivier understandingthedynamicofpomsinfectionandtheroleofmicrobiotacompositioninthesurvivalofpacificoysterscrassostreagigas
AT hiltonzoe understandingthedynamicofpomsinfectionandtheroleofmicrobiotacompositioninthesurvivalofpacificoysterscrassostreagigas
AT burguinjeanfrancois understandingthedynamicofpomsinfectionandtheroleofmicrobiotacompositioninthesurvivalofpacificoysterscrassostreagigas
AT roltonanne understandingthedynamicofpomsinfectionandtheroleofmicrobiotacompositioninthesurvivalofpacificoysterscrassostreagigas
AT berryjolene understandingthedynamicofpomsinfectionandtheroleofmicrobiotacompositioninthesurvivalofpacificoysterscrassostreagigas
AT pochonxavier understandingthedynamicofpomsinfectionandtheroleofmicrobiotacompositioninthesurvivalofpacificoysterscrassostreagigas
AT boudrypierre understandingthedynamicofpomsinfectionandtheroleofmicrobiotacompositioninthesurvivalofpacificoysterscrassostreagigas
AT vignierjulien understandingthedynamicofpomsinfectionandtheroleofmicrobiotacompositioninthesurvivalofpacificoysterscrassostreagigas