Increased growth metabolism promotes viral infection in a susceptible oyster population
International audience The magnitude of an epidemic depends on host susceptibility to the disease, a trait influenced by the genetic constitution of the host and its environment. While the genetic basis of disease susceptibility is often associated with immune capacities, environmental effects gener...
Published in: | Aquaculture Environment Interactions |
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Main Authors: | , , , |
Other Authors: | , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
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HAL CCSD
2023
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Subjects: | |
Online Access: | https://hal.univ-brest.fr/hal-04056707 https://hal.univ-brest.fr/hal-04056707/document https://hal.univ-brest.fr/hal-04056707/file/99715.pdf https://doi.org/10.3354/aei00450 |
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Open Polar |
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Institut national des sciences de l'Univers: HAL-INSU |
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ftinsu |
language |
English |
topic |
[SDV.SA.SPA]Life Sciences [q-bio]/Agricultural sciences/Animal production studies |
spellingShingle |
[SDV.SA.SPA]Life Sciences [q-bio]/Agricultural sciences/Animal production studies Petton, Bruno Alunno-Bruscia, Marianne Mitta, Guillaume Pernet, Fabrice Increased growth metabolism promotes viral infection in a susceptible oyster population |
topic_facet |
[SDV.SA.SPA]Life Sciences [q-bio]/Agricultural sciences/Animal production studies |
description |
International audience The magnitude of an epidemic depends on host susceptibility to the disease, a trait influenced by the genetic constitution of the host and its environment. While the genetic basis of disease susceptibility is often associated with immune capacities, environmental effects generally reflect complex physiological trade-offs. We suggest here that in the case of obligate pathogens whose proliferation depends on the cellular machinery of the host (e.g. viruses), disease susceptibility is directly influenced by host growth. To test our hypothesis, we focussed on a viral disease affecting an ecologically relevant model exploited worldwide, the Pacific oyster Crassostrea gigas. Oysters originating from 3 lines with contrasting resistance to the disease were divided into 3 groups displaying different growth rates and acclimated to 3 food levels and 2 temperatures to generate different growth rates. These oysters were then exposed to the virus, and survival and viral shedding were measured. Finally, we developed a risk model to rank the relative importance of temperature, food, genetic selection and growth on disease-induced mortality. We found that increasing growth through temperature, food level or selection of fast-growing animals all increased mortality, especially in host populations where susceptible phenotypes dominated. Food provisioning was the most influential factor associated with higher viral shedding, followed by temperature, resistance phenotype and growth rate. We suggest that growth-forcing factors may promote the development of obligate intracellular pathogens and epidemic risk, thus opening up avenues for disease management based on the manipulation of host metabolism. |
author2 |
Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Ecosystèmes Insulaires Océaniens (UMR 241) (EIO) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de la Polynésie Française (UPF)-Institut Louis Malardé Papeete (ILM) Institut de Recherche pour le Développement (IRD) ANR-16-CE32-0008,REVENGE,L'huître comme niche de l'évolution et l'émergence de vibrios pathogènes(2016) |
format |
Article in Journal/Newspaper |
author |
Petton, Bruno Alunno-Bruscia, Marianne Mitta, Guillaume Pernet, Fabrice |
author_facet |
Petton, Bruno Alunno-Bruscia, Marianne Mitta, Guillaume Pernet, Fabrice |
author_sort |
Petton, Bruno |
title |
Increased growth metabolism promotes viral infection in a susceptible oyster population |
title_short |
Increased growth metabolism promotes viral infection in a susceptible oyster population |
title_full |
Increased growth metabolism promotes viral infection in a susceptible oyster population |
title_fullStr |
Increased growth metabolism promotes viral infection in a susceptible oyster population |
title_full_unstemmed |
Increased growth metabolism promotes viral infection in a susceptible oyster population |
title_sort |
increased growth metabolism promotes viral infection in a susceptible oyster population |
publisher |
HAL CCSD |
publishDate |
2023 |
url |
https://hal.univ-brest.fr/hal-04056707 https://hal.univ-brest.fr/hal-04056707/document https://hal.univ-brest.fr/hal-04056707/file/99715.pdf https://doi.org/10.3354/aei00450 |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
Crassostrea gigas Pacific oyster |
genre_facet |
Crassostrea gigas Pacific oyster |
op_source |
ISSN: 1869-215X Aquaculture Environment Interactions https://hal.univ-brest.fr/hal-04056707 Aquaculture Environment Interactions, 2023, 15, pp.19 - 33. ⟨10.3354/aei00450⟩ |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.3354/aei00450 hal-04056707 https://hal.univ-brest.fr/hal-04056707 https://hal.univ-brest.fr/hal-04056707/document https://hal.univ-brest.fr/hal-04056707/file/99715.pdf doi:10.3354/aei00450 |
op_rights |
info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.3354/aei00450 |
container_title |
Aquaculture Environment Interactions |
container_volume |
15 |
container_start_page |
19 |
op_container_end_page |
33 |
_version_ |
1796308398434680832 |
spelling |
ftinsu:oai:HAL:hal-04056707v1 2024-04-14T08:10:45+00:00 Increased growth metabolism promotes viral infection in a susceptible oyster population Petton, Bruno Alunno-Bruscia, Marianne Mitta, Guillaume Pernet, Fabrice Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Ecosystèmes Insulaires Océaniens (UMR 241) (EIO) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de la Polynésie Française (UPF)-Institut Louis Malardé Papeete (ILM) Institut de Recherche pour le Développement (IRD) ANR-16-CE32-0008,REVENGE,L'huître comme niche de l'évolution et l'émergence de vibrios pathogènes(2016) 2023-02-02 https://hal.univ-brest.fr/hal-04056707 https://hal.univ-brest.fr/hal-04056707/document https://hal.univ-brest.fr/hal-04056707/file/99715.pdf https://doi.org/10.3354/aei00450 en eng HAL CCSD Inter-reseach science publisher info:eu-repo/semantics/altIdentifier/doi/10.3354/aei00450 hal-04056707 https://hal.univ-brest.fr/hal-04056707 https://hal.univ-brest.fr/hal-04056707/document https://hal.univ-brest.fr/hal-04056707/file/99715.pdf doi:10.3354/aei00450 info:eu-repo/semantics/OpenAccess ISSN: 1869-215X Aquaculture Environment Interactions https://hal.univ-brest.fr/hal-04056707 Aquaculture Environment Interactions, 2023, 15, pp.19 - 33. ⟨10.3354/aei00450⟩ [SDV.SA.SPA]Life Sciences [q-bio]/Agricultural sciences/Animal production studies info:eu-repo/semantics/article Journal articles 2023 ftinsu https://doi.org/10.3354/aei00450 2024-03-21T17:08:37Z International audience The magnitude of an epidemic depends on host susceptibility to the disease, a trait influenced by the genetic constitution of the host and its environment. While the genetic basis of disease susceptibility is often associated with immune capacities, environmental effects generally reflect complex physiological trade-offs. We suggest here that in the case of obligate pathogens whose proliferation depends on the cellular machinery of the host (e.g. viruses), disease susceptibility is directly influenced by host growth. To test our hypothesis, we focussed on a viral disease affecting an ecologically relevant model exploited worldwide, the Pacific oyster Crassostrea gigas. Oysters originating from 3 lines with contrasting resistance to the disease were divided into 3 groups displaying different growth rates and acclimated to 3 food levels and 2 temperatures to generate different growth rates. These oysters were then exposed to the virus, and survival and viral shedding were measured. Finally, we developed a risk model to rank the relative importance of temperature, food, genetic selection and growth on disease-induced mortality. We found that increasing growth through temperature, food level or selection of fast-growing animals all increased mortality, especially in host populations where susceptible phenotypes dominated. Food provisioning was the most influential factor associated with higher viral shedding, followed by temperature, resistance phenotype and growth rate. We suggest that growth-forcing factors may promote the development of obligate intracellular pathogens and epidemic risk, thus opening up avenues for disease management based on the manipulation of host metabolism. Article in Journal/Newspaper Crassostrea gigas Pacific oyster Institut national des sciences de l'Univers: HAL-INSU Pacific Aquaculture Environment Interactions 15 19 33 |