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...

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Published in:Aquaculture Environment Interactions
Main Authors: Petton, Bruno, Alunno-Bruscia, Marianne, Mitta, Guillaume, Pernet, Fabrice
Other Authors: 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
Language:English
Published: HAL CCSD 2023
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
id ftanrparis:oai:HAL:hal-04056707v1
record_format openpolar
institution Open Polar
collection Portail HAL-ANR (Agence Nationale de la Recherche)
op_collection_id ftanrparis
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
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
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spelling ftanrparis:oai:HAL:hal-04056707v1 2024-04-21T08:00:46+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 ftanrparis https://doi.org/10.3354/aei00450 2024-03-26T18:12:23Z 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 Portail HAL-ANR (Agence Nationale de la Recherche) Aquaculture Environment Interactions 15 19 33