Increased growth metabolism promotes viral infection in a susceptible oyster population

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 ph...

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Published in:Aquaculture Environment Interactions
Main Authors: Petton, Bruno, Alunno-bruscia, Marianne, Mitta, Guillaume, Pernet, Fabrice
Format: Article in Journal/Newspaper
Language:English
Published: Inter-Research Science Center 2023
Subjects:
Online Access:https://archimer.ifremer.fr/doc/00819/93142/99715.pdf
https://archimer.ifremer.fr/doc/00819/93142/99716.pdf
https://doi.org/10.3354/aei00450
https://archimer.ifremer.fr/doc/00819/93142/
id ftarchimer:oai:archimer.ifremer.fr:93142
record_format openpolar
spelling ftarchimer:oai:archimer.ifremer.fr:93142 2023-05-15T15:58:53+02:00 Increased growth metabolism promotes viral infection in a susceptible oyster population Petton, Bruno Alunno-bruscia, Marianne Mitta, Guillaume Pernet, Fabrice 2023-02-02 application/pdf https://archimer.ifremer.fr/doc/00819/93142/99715.pdf https://archimer.ifremer.fr/doc/00819/93142/99716.pdf https://doi.org/10.3354/aei00450 https://archimer.ifremer.fr/doc/00819/93142/ eng eng Inter-Research Science Center https://archimer.ifremer.fr/doc/00819/93142/99715.pdf https://archimer.ifremer.fr/doc/00819/93142/99716.pdf doi:10.3354/aei00450 https://archimer.ifremer.fr/doc/00819/93142/ info:eu-repo/semantics/openAccess restricted use Aquaculture Environment Interactions (1869-215X) (Inter-Research Science Center), 2023-02-02 , Vol. 15 , P. 19-33 Epidemiology Growth · Health Metabolism Physiological trade-off Temperature text Publication info:eu-repo/semantics/article 2023 ftarchimer https://doi.org/10.3354/aei00450 2023-02-07T23:52:15Z 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 Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer) Pacific Aquaculture Environment Interactions 15 19 33
institution Open Polar
collection Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer)
op_collection_id ftarchimer
language English
topic Epidemiology
Growth · Health
Metabolism
Physiological trade-off
Temperature
spellingShingle Epidemiology
Growth · Health
Metabolism
Physiological trade-off
Temperature
Petton, Bruno
Alunno-bruscia, Marianne
Mitta, Guillaume
Pernet, Fabrice
Increased growth metabolism promotes viral infection in a susceptible oyster population
topic_facet Epidemiology
Growth · Health
Metabolism
Physiological trade-off
Temperature
description 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.
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 Inter-Research Science Center
publishDate 2023
url https://archimer.ifremer.fr/doc/00819/93142/99715.pdf
https://archimer.ifremer.fr/doc/00819/93142/99716.pdf
https://doi.org/10.3354/aei00450
https://archimer.ifremer.fr/doc/00819/93142/
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source Aquaculture Environment Interactions (1869-215X) (Inter-Research Science Center), 2023-02-02 , Vol. 15 , P. 19-33
op_relation https://archimer.ifremer.fr/doc/00819/93142/99715.pdf
https://archimer.ifremer.fr/doc/00819/93142/99716.pdf
doi:10.3354/aei00450
https://archimer.ifremer.fr/doc/00819/93142/
op_rights info:eu-repo/semantics/openAccess
restricted use
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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