Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses

Abstract Background The impact of the microbiota on host fitness has so far mainly been demonstrated for the bacterial microbiome. We know much less about host-associated protist and viral communities, largely due to technical issues. However, all microorganisms within a microbiome potentially inter...

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Published in:Animal Microbiome
Main Authors: S. Dupont, A. Lokmer, E. Corre, J.-C. Auguet, B. Petton, E. Toulza, C. Montagnani, G. Tanguy, D. Pecqueur, C. Salmeron, L. Guillou, C. Desnues, B. La Scola, J. Bou Khalil, J. de Lorgeril, G. Mitta, Y. Gueguen, J.-M. Escoubas
Format: Article in Journal/Newspaper
Language:English
Published: BMC 2020
Subjects:
Online Access:https://doi.org/10.1186/s42523-020-00032-w
https://doaj.org/article/332aa399e65644198c7d00a25a1c5751
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spelling ftdoajarticles:oai:doaj.org/article:332aa399e65644198c7d00a25a1c5751 2023-05-15T15:59:02+02:00 Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses S. Dupont A. Lokmer E. Corre J.-C. Auguet B. Petton E. Toulza C. Montagnani G. Tanguy D. Pecqueur C. Salmeron L. Guillou C. Desnues B. La Scola J. Bou Khalil J. de Lorgeril G. Mitta Y. Gueguen J.-M. Escoubas 2020-04-01T00:00:00Z https://doi.org/10.1186/s42523-020-00032-w https://doaj.org/article/332aa399e65644198c7d00a25a1c5751 EN eng BMC http://link.springer.com/article/10.1186/s42523-020-00032-w https://doaj.org/toc/2524-4671 doi:10.1186/s42523-020-00032-w 2524-4671 https://doaj.org/article/332aa399e65644198c7d00a25a1c5751 Animal Microbiome, Vol 2, Iss 1, Pp 1-16 (2020) Oyster genetic background Hemolymph microbiota dynamics Early-life microbiota Trans-kingdom interactions Crassostrea gigas Within-host ecosystem Veterinary medicine SF600-1100 Microbiology QR1-502 article 2020 ftdoajarticles https://doi.org/10.1186/s42523-020-00032-w 2022-12-31T08:27:16Z Abstract Background The impact of the microbiota on host fitness has so far mainly been demonstrated for the bacterial microbiome. We know much less about host-associated protist and viral communities, largely due to technical issues. However, all microorganisms within a microbiome potentially interact with each other as well as with the host and the environment, therefore likely affecting the host health. Results We set out to explore how environmental and host factors shape the composition and diversity of bacterial, protist and viral microbial communities in the Pacific oyster hemolymph, both in health and disease. To do so, five oyster families differing in susceptibility to the Pacific oyster mortality syndrome were reared in hatchery and transplanted into a natural environment either before or during a disease outbreak. Using metabarcoding and shotgun metagenomics, we demonstrate that hemolymph can be considered as an ecological niche hosting bacterial, protist and viral communities, each of them shaped by different factors and distinct from the corresponding communities in the surrounding seawater. Overall, we found that hemolymph microbiota is more strongly shaped by the environment than by host genetic background. Co-occurrence network analyses suggest a disruption of the microbial network after transplantation into natural environment during both non-infectious and infectious periods. Whereas we could not identify a common microbial community signature for healthy animals, OsHV-1 μVar virus dominated the hemolymph virome during the disease outbreak, without significant modifications of other microbiota components. Conclusion Our study shows that oyster hemolymph is a complex ecosystem containing diverse bacteria, protists and viruses, whose composition and dynamics are primarily determined by the environment. However, all of these are also shaped by oyster genetic backgrounds, indicating they indeed interact with the oyster host and are therefore not only of transient character. Although it seems that ... Article in Journal/Newspaper Crassostrea gigas Pacific oyster Directory of Open Access Journals: DOAJ Articles Pacific Animal Microbiome 2 1
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Oyster genetic background
Hemolymph microbiota dynamics
Early-life microbiota
Trans-kingdom interactions
Crassostrea gigas
Within-host ecosystem
Veterinary medicine
SF600-1100
Microbiology
QR1-502
spellingShingle Oyster genetic background
Hemolymph microbiota dynamics
Early-life microbiota
Trans-kingdom interactions
Crassostrea gigas
Within-host ecosystem
Veterinary medicine
SF600-1100
Microbiology
QR1-502
S. Dupont
A. Lokmer
E. Corre
J.-C. Auguet
B. Petton
E. Toulza
C. Montagnani
G. Tanguy
D. Pecqueur
C. Salmeron
L. Guillou
C. Desnues
B. La Scola
J. Bou Khalil
J. de Lorgeril
G. Mitta
Y. Gueguen
J.-M. Escoubas
Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses
topic_facet Oyster genetic background
Hemolymph microbiota dynamics
Early-life microbiota
Trans-kingdom interactions
Crassostrea gigas
Within-host ecosystem
Veterinary medicine
SF600-1100
Microbiology
QR1-502
description Abstract Background The impact of the microbiota on host fitness has so far mainly been demonstrated for the bacterial microbiome. We know much less about host-associated protist and viral communities, largely due to technical issues. However, all microorganisms within a microbiome potentially interact with each other as well as with the host and the environment, therefore likely affecting the host health. Results We set out to explore how environmental and host factors shape the composition and diversity of bacterial, protist and viral microbial communities in the Pacific oyster hemolymph, both in health and disease. To do so, five oyster families differing in susceptibility to the Pacific oyster mortality syndrome were reared in hatchery and transplanted into a natural environment either before or during a disease outbreak. Using metabarcoding and shotgun metagenomics, we demonstrate that hemolymph can be considered as an ecological niche hosting bacterial, protist and viral communities, each of them shaped by different factors and distinct from the corresponding communities in the surrounding seawater. Overall, we found that hemolymph microbiota is more strongly shaped by the environment than by host genetic background. Co-occurrence network analyses suggest a disruption of the microbial network after transplantation into natural environment during both non-infectious and infectious periods. Whereas we could not identify a common microbial community signature for healthy animals, OsHV-1 μVar virus dominated the hemolymph virome during the disease outbreak, without significant modifications of other microbiota components. Conclusion Our study shows that oyster hemolymph is a complex ecosystem containing diverse bacteria, protists and viruses, whose composition and dynamics are primarily determined by the environment. However, all of these are also shaped by oyster genetic backgrounds, indicating they indeed interact with the oyster host and are therefore not only of transient character. Although it seems that ...
format Article in Journal/Newspaper
author S. Dupont
A. Lokmer
E. Corre
J.-C. Auguet
B. Petton
E. Toulza
C. Montagnani
G. Tanguy
D. Pecqueur
C. Salmeron
L. Guillou
C. Desnues
B. La Scola
J. Bou Khalil
J. de Lorgeril
G. Mitta
Y. Gueguen
J.-M. Escoubas
author_facet S. Dupont
A. Lokmer
E. Corre
J.-C. Auguet
B. Petton
E. Toulza
C. Montagnani
G. Tanguy
D. Pecqueur
C. Salmeron
L. Guillou
C. Desnues
B. La Scola
J. Bou Khalil
J. de Lorgeril
G. Mitta
Y. Gueguen
J.-M. Escoubas
author_sort S. Dupont
title Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses
title_short Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses
title_full Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses
title_fullStr Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses
title_full_unstemmed Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses
title_sort oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses
publisher BMC
publishDate 2020
url https://doi.org/10.1186/s42523-020-00032-w
https://doaj.org/article/332aa399e65644198c7d00a25a1c5751
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source Animal Microbiome, Vol 2, Iss 1, Pp 1-16 (2020)
op_relation http://link.springer.com/article/10.1186/s42523-020-00032-w
https://doaj.org/toc/2524-4671
doi:10.1186/s42523-020-00032-w
2524-4671
https://doaj.org/article/332aa399e65644198c7d00a25a1c5751
op_doi https://doi.org/10.1186/s42523-020-00032-w
container_title Animal Microbiome
container_volume 2
container_issue 1
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