Antiviral protection in the Pacific oyster Crassostrea (Magallana) gigas against OsHV-1 infection using UV-inactivated virus

International audience The increase of the frequency and severity of marine diseases affecting farmed marine mollusks are currently threatening the sustainability of this aquaculture sector, with few available prophylactic or therapeutic solutions. Recent advances have shown that the innate immune s...

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Main Authors: Morga, Benjamin, Mège, Mickäel, Faury, Nicole, Dégremont, Lionel, Petton, Bruno, Pépin, Jean-François, Renault, Tristan, Montagnani, C.
Other Authors: Unité Adaptation et Santé des Invertébrés Marins (ASIM), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), 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), Laboratoire Environnement Ressources des Pertuis Charentais (LERPC), Unité Littoral (LITTORAL), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), Interactions Hôtes-Pathogènes-Environnements (IHPE), Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), ANR-19-CE20-0004,DECICOMP,Déchiffrer toute la complexité du syndrome de mortalité des huîtres du Pacifique pour modéliser le risque épidémiologique.(2019)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2024
Subjects:
Online Access:https://hal.science/hal-04556469
https://hal.science/hal-04556469/document
https://hal.science/hal-04556469/file/Morga-2024-FrontiersMarBiol-Antiviral.pdf
https://doi.org/10.3389/fmars.2024.1378511
id ftunivbrest:oai:HAL:hal-04556469v1
record_format openpolar
institution Open Polar
collection Université de Bretagne Occidentale: HAL
op_collection_id ftunivbrest
language English
topic Crassostrea gigas
Magallana gigas
Pacific oyster
antiviral
immunity
priming
OsHV-1
invertebrate
[SDV.BA.MVSA]Life Sciences [q-bio]/Animal biology/Veterinary medicine and animal Health
[SDV.IMM.VAC]Life Sciences [q-bio]/Immunology/Vaccinology
[SDV.SA.ZOO]Life Sciences [q-bio]/Agricultural sciences/Zootechny
spellingShingle Crassostrea gigas
Magallana gigas
Pacific oyster
antiviral
immunity
priming
OsHV-1
invertebrate
[SDV.BA.MVSA]Life Sciences [q-bio]/Animal biology/Veterinary medicine and animal Health
[SDV.IMM.VAC]Life Sciences [q-bio]/Immunology/Vaccinology
[SDV.SA.ZOO]Life Sciences [q-bio]/Agricultural sciences/Zootechny
Morga, Benjamin
Mège, Mickäel
Faury, Nicole
Dégremont, Lionel
Petton, Bruno
Pépin, Jean-François
Renault, Tristan
Montagnani, C.
Antiviral protection in the Pacific oyster Crassostrea (Magallana) gigas against OsHV-1 infection using UV-inactivated virus
topic_facet Crassostrea gigas
Magallana gigas
Pacific oyster
antiviral
immunity
priming
OsHV-1
invertebrate
[SDV.BA.MVSA]Life Sciences [q-bio]/Animal biology/Veterinary medicine and animal Health
[SDV.IMM.VAC]Life Sciences [q-bio]/Immunology/Vaccinology
[SDV.SA.ZOO]Life Sciences [q-bio]/Agricultural sciences/Zootechny
description International audience The increase of the frequency and severity of marine diseases affecting farmed marine mollusks are currently threatening the sustainability of this aquaculture sector, with few available prophylactic or therapeutic solutions. Recent advances have shown that the innate immune system of invertebrates can develop memory mechanisms allowing for efficient protection against pathogens. These properties have been called innate immune memory, immune priming or trained immunity. Previous results demonstrated the possibility to elicit antiviral immune priming to protect Pacific oysters against the ostreid herpes virus 1 (OsHV-1), currently plaguing M. gigas production worldwide. Here, we demonstrate that UV-inactivated OsHV-1 is also a potent elicitor of immune priming. Previous exposure to the inactivated virus was able to efficiently protect oysters against OsHV-1, significantly increasing oyster survival. We demonstrate that this exposure blocked viral replication and was able to induce antiviral gene expression potentially involved in controlling the infection. Finally, we show that this phenomenon can persist for at least 3 months, suggesting the induction of innate immune memory mechanisms. This study unravels new ways to train the Pacific oyster immune system that could represent an opportunity to develop new prophylactic strategies to improve health and to sustain the development of marine mollusk aquaculture.
author2 Unité Adaptation et Santé des Invertébrés Marins (ASIM)
Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)
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)
Laboratoire Environnement Ressources des Pertuis Charentais (LERPC)
Unité Littoral (LITTORAL)
Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)
Interactions Hôtes-Pathogènes-Environnements (IHPE)
Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)
ANR-19-CE20-0004,DECICOMP,Déchiffrer toute la complexité du syndrome de mortalité des huîtres du Pacifique pour modéliser le risque épidémiologique.(2019)
format Article in Journal/Newspaper
author Morga, Benjamin
Mège, Mickäel
Faury, Nicole
Dégremont, Lionel
Petton, Bruno
Pépin, Jean-François
Renault, Tristan
Montagnani, C.
author_facet Morga, Benjamin
Mège, Mickäel
Faury, Nicole
Dégremont, Lionel
Petton, Bruno
Pépin, Jean-François
Renault, Tristan
Montagnani, C.
author_sort Morga, Benjamin
title Antiviral protection in the Pacific oyster Crassostrea (Magallana) gigas against OsHV-1 infection using UV-inactivated virus
title_short Antiviral protection in the Pacific oyster Crassostrea (Magallana) gigas against OsHV-1 infection using UV-inactivated virus
title_full Antiviral protection in the Pacific oyster Crassostrea (Magallana) gigas against OsHV-1 infection using UV-inactivated virus
title_fullStr Antiviral protection in the Pacific oyster Crassostrea (Magallana) gigas against OsHV-1 infection using UV-inactivated virus
title_full_unstemmed Antiviral protection in the Pacific oyster Crassostrea (Magallana) gigas against OsHV-1 infection using UV-inactivated virus
title_sort antiviral protection in the pacific oyster crassostrea (magallana) gigas against oshv-1 infection using uv-inactivated virus
publisher HAL CCSD
publishDate 2024
url https://hal.science/hal-04556469
https://hal.science/hal-04556469/document
https://hal.science/hal-04556469/file/Morga-2024-FrontiersMarBiol-Antiviral.pdf
https://doi.org/10.3389/fmars.2024.1378511
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source ISSN: 2296-7745
Frontiers in Marine Science
https://hal.science/hal-04556469
Frontiers in Marine Science, 2024, 11, pp.1378511. ⟨10.3389/fmars.2024.1378511⟩
https://www.frontiersin.org/articles/10.3389/fmars.2024.1378511/full?&utm_source=Email_to_authors_&utm_medium=Email&utm_content=T1_11.5e1_author&utm_campaign=Email_publication&field=&journalName=Frontiers_in_Marine_Science&id=1378511
op_relation info:eu-repo/semantics/altIdentifier/doi/10.3389/fmars.2024.1378511
hal-04556469
https://hal.science/hal-04556469
https://hal.science/hal-04556469/document
https://hal.science/hal-04556469/file/Morga-2024-FrontiersMarBiol-Antiviral.pdf
doi:10.3389/fmars.2024.1378511
op_rights info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.3389/fmars.2024.137851110.3389/fmars.2024.1378511/full
_version_ 1799478884693966848
spelling ftunivbrest:oai:HAL:hal-04556469v1 2024-05-19T07:39:19+00:00 Antiviral protection in the Pacific oyster Crassostrea (Magallana) gigas against OsHV-1 infection using UV-inactivated virus Morga, Benjamin Mège, Mickäel Faury, Nicole Dégremont, Lionel Petton, Bruno Pépin, Jean-François Renault, Tristan Montagnani, C. Unité Adaptation et Santé des Invertébrés Marins (ASIM) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) 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) Laboratoire Environnement Ressources des Pertuis Charentais (LERPC) Unité Littoral (LITTORAL) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Interactions Hôtes-Pathogènes-Environnements (IHPE) Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM) ANR-19-CE20-0004,DECICOMP,Déchiffrer toute la complexité du syndrome de mortalité des huîtres du Pacifique pour modéliser le risque épidémiologique.(2019) 2024 https://hal.science/hal-04556469 https://hal.science/hal-04556469/document https://hal.science/hal-04556469/file/Morga-2024-FrontiersMarBiol-Antiviral.pdf https://doi.org/10.3389/fmars.2024.1378511 en eng HAL CCSD Frontiers Media info:eu-repo/semantics/altIdentifier/doi/10.3389/fmars.2024.1378511 hal-04556469 https://hal.science/hal-04556469 https://hal.science/hal-04556469/document https://hal.science/hal-04556469/file/Morga-2024-FrontiersMarBiol-Antiviral.pdf doi:10.3389/fmars.2024.1378511 info:eu-repo/semantics/OpenAccess ISSN: 2296-7745 Frontiers in Marine Science https://hal.science/hal-04556469 Frontiers in Marine Science, 2024, 11, pp.1378511. ⟨10.3389/fmars.2024.1378511⟩ https://www.frontiersin.org/articles/10.3389/fmars.2024.1378511/full?&utm_source=Email_to_authors_&utm_medium=Email&utm_content=T1_11.5e1_author&utm_campaign=Email_publication&field=&journalName=Frontiers_in_Marine_Science&id=1378511 Crassostrea gigas Magallana gigas Pacific oyster antiviral immunity priming OsHV-1 invertebrate [SDV.BA.MVSA]Life Sciences [q-bio]/Animal biology/Veterinary medicine and animal Health [SDV.IMM.VAC]Life Sciences [q-bio]/Immunology/Vaccinology [SDV.SA.ZOO]Life Sciences [q-bio]/Agricultural sciences/Zootechny info:eu-repo/semantics/article Journal articles 2024 ftunivbrest https://doi.org/10.3389/fmars.2024.137851110.3389/fmars.2024.1378511/full 2024-05-01T23:48:47Z International audience The increase of the frequency and severity of marine diseases affecting farmed marine mollusks are currently threatening the sustainability of this aquaculture sector, with few available prophylactic or therapeutic solutions. Recent advances have shown that the innate immune system of invertebrates can develop memory mechanisms allowing for efficient protection against pathogens. These properties have been called innate immune memory, immune priming or trained immunity. Previous results demonstrated the possibility to elicit antiviral immune priming to protect Pacific oysters against the ostreid herpes virus 1 (OsHV-1), currently plaguing M. gigas production worldwide. Here, we demonstrate that UV-inactivated OsHV-1 is also a potent elicitor of immune priming. Previous exposure to the inactivated virus was able to efficiently protect oysters against OsHV-1, significantly increasing oyster survival. We demonstrate that this exposure blocked viral replication and was able to induce antiviral gene expression potentially involved in controlling the infection. Finally, we show that this phenomenon can persist for at least 3 months, suggesting the induction of innate immune memory mechanisms. This study unravels new ways to train the Pacific oyster immune system that could represent an opportunity to develop new prophylactic strategies to improve health and to sustain the development of marine mollusk aquaculture. Article in Journal/Newspaper Crassostrea gigas Pacific oyster Université de Bretagne Occidentale: HAL