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: Dupont, S., Lokmer, A., Corre, E., Auguet, J.-C., Petton, B., Toulza, E., Montagnani, C., Tanguy, G., Pecqueur, D., Salmeron, C., Guillou, L., Desnues, C., La Scola, B., Bou Khalil, J., de Lorgeril, J., Mitta, G., Gueguen, Y., Escoubas, J.-M.
Other Authors: Horizon 2020, Agence Nationale de la Recherche
Format: Article in Journal/Newspaper
Language:English
Published: Springer Science and Business Media LLC 2020
Subjects:
Online Access:http://dx.doi.org/10.1186/s42523-020-00032-w
https://link.springer.com/content/pdf/10.1186/s42523-020-00032-w.pdf
https://link.springer.com/article/10.1186/s42523-020-00032-w/fulltext.html
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spelling crspringernat:10.1186/s42523-020-00032-w 2023-05-15T17:54:18+02:00 Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses Dupont, S. Lokmer, A. Corre, E. Auguet, J.-C. Petton, B. Toulza, E. Montagnani, C. Tanguy, G. Pecqueur, D. Salmeron, C. Guillou, L. Desnues, C. La Scola, B. Bou Khalil, J. de Lorgeril, J. Mitta, G. Gueguen, Y. Escoubas, J.-M. Horizon 2020 Agence Nationale de la Recherche 2020 http://dx.doi.org/10.1186/s42523-020-00032-w https://link.springer.com/content/pdf/10.1186/s42523-020-00032-w.pdf https://link.springer.com/article/10.1186/s42523-020-00032-w/fulltext.html en eng Springer Science and Business Media LLC https://creativecommons.org/licenses/by/4.0 https://creativecommons.org/licenses/by/4.0 CC-BY Animal Microbiome volume 2, issue 1 ISSN 2524-4671 journal-article 2020 crspringernat https://doi.org/10.1186/s42523-020-00032-w 2022-01-04T15:31:02Z 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 the three microbiome components respond independently to environmental conditions, better characterization of hemolymph-associated viruses could change this picture. Article in Journal/Newspaper Pacific oyster Springer Nature (via Crossref) Pacific Animal Microbiome 2 1
institution Open Polar
collection Springer Nature (via Crossref)
op_collection_id crspringernat
language English
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 the three microbiome components respond independently to environmental conditions, better characterization of hemolymph-associated viruses could change this picture.
author2 Horizon 2020
Agence Nationale de la Recherche
format Article in Journal/Newspaper
author Dupont, S.
Lokmer, A.
Corre, E.
Auguet, J.-C.
Petton, B.
Toulza, E.
Montagnani, C.
Tanguy, G.
Pecqueur, D.
Salmeron, C.
Guillou, L.
Desnues, C.
La Scola, B.
Bou Khalil, J.
de Lorgeril, J.
Mitta, G.
Gueguen, Y.
Escoubas, J.-M.
spellingShingle Dupont, S.
Lokmer, A.
Corre, E.
Auguet, J.-C.
Petton, B.
Toulza, E.
Montagnani, C.
Tanguy, G.
Pecqueur, D.
Salmeron, C.
Guillou, L.
Desnues, C.
La Scola, B.
Bou Khalil, J.
de Lorgeril, J.
Mitta, G.
Gueguen, Y.
Escoubas, J.-M.
Oyster hemolymph is a complex and dynamic ecosystem hosting bacteria, protists and viruses
author_facet Dupont, S.
Lokmer, A.
Corre, E.
Auguet, J.-C.
Petton, B.
Toulza, E.
Montagnani, C.
Tanguy, G.
Pecqueur, D.
Salmeron, C.
Guillou, L.
Desnues, C.
La Scola, B.
Bou Khalil, J.
de Lorgeril, J.
Mitta, G.
Gueguen, Y.
Escoubas, J.-M.
author_sort Dupont, S.
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 Springer Science and Business Media LLC
publishDate 2020
url http://dx.doi.org/10.1186/s42523-020-00032-w
https://link.springer.com/content/pdf/10.1186/s42523-020-00032-w.pdf
https://link.springer.com/article/10.1186/s42523-020-00032-w/fulltext.html
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geographic_facet Pacific
genre Pacific oyster
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op_source Animal Microbiome
volume 2, issue 1
ISSN 2524-4671
op_rights https://creativecommons.org/licenses/by/4.0
https://creativecommons.org/licenses/by/4.0
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op_doi https://doi.org/10.1186/s42523-020-00032-w
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