Transcriptome analysis reveals strong and complex antiviral response in a mollusc

International audience Viruses are highly abundant in the oceans, and how filter-feeding molluscs without adaptive immunity defend themselves against viruses is not well understood. We studied the response of a mollusc Crassostrea gigas to Ostreid herpesvirus 1 µVar (OsHV-1μVar) infections using tra...

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Published in:Fish & Shellfish Immunology
Main Authors: He, Yan, Jouaux, Aude, Ford, Susan, E., Lelong, Christophe, Sourdaine, Pascal, Mathieu, Michel, Guo, Ximing
Other Authors: Ocean University of China (OUC), Rutgers University System (Rutgers), Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2015
Subjects:
Online Access:https://normandie-univ.hal.science/hal-02296483
https://doi.org/10.1016/j.fsi.2015.05.023
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spelling ftsorbonneuniv:oai:HAL:hal-02296483v1 2023-12-17T10:29:17+01:00 Transcriptome analysis reveals strong and complex antiviral response in a mollusc He, Yan Jouaux, Aude Ford, Susan, E. Lelong, Christophe Sourdaine, Pascal Mathieu, Michel Guo, Ximing Ocean University of China (OUC) Rutgers University System (Rutgers) Biologie des Organismes et Ecosystèmes Aquatiques (BOREA) Université de Caen Normandie (UNICAEN) Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA) 2015-09 https://normandie-univ.hal.science/hal-02296483 https://doi.org/10.1016/j.fsi.2015.05.023 en eng HAL CCSD Elsevier info:eu-repo/semantics/altIdentifier/doi/10.1016/j.fsi.2015.05.023 hal-02296483 https://normandie-univ.hal.science/hal-02296483 doi:10.1016/j.fsi.2015.05.023 ISSN: 1050-4648 EISSN: 1095-9947 Fish and Shellfish Immunology https://normandie-univ.hal.science/hal-02296483 Fish and Shellfish Immunology, 2015, 46 (1), pp.131-144. ⟨10.1016/j.fsi.2015.05.023⟩ Marine virus Ostreid herpesvirus OsHV-1μVar Immune receptors Antiviral response Innate immunity Viral RNA Oyster Oxidative burst [SDV]Life Sciences [q-bio] info:eu-repo/semantics/article Journal articles 2015 ftsorbonneuniv https://doi.org/10.1016/j.fsi.2015.05.023 2023-11-21T23:50:49Z International audience Viruses are highly abundant in the oceans, and how filter-feeding molluscs without adaptive immunity defend themselves against viruses is not well understood. We studied the response of a mollusc Crassostrea gigas to Ostreid herpesvirus 1 µVar (OsHV-1μVar) infections using transcriptome sequencing. OsHV-1μVar can replicate extremely rapidly after challenge of C. gigas as evidenced by explosive viral transcription and DNA synthesis, which peaked at 24 and 48 h post-inoculation, respectively, accompanied by heavy oyster mortalities. At 120 h post-injection, however, viral gene transcription and DNA load, and oyster mortality, were greatly reduced indicating an end of active infections and effective control of viral replication in surviving oysters. Transcriptome analysis of the host revealed strong and complex responses involving the activation of all major innate immune pathways that are equipped with expanded and often novel receptors and adaptors. Novel Toll-like receptor (TLR) and MyD88-like genes lacking essential domains were highly up-regulated in the oyster, possibly interfering with TLR signal transduction. RIG-1/MDA5 receptors for viral RNA, interferon-regulatory factors, tissue necrosis factors and interleukin-17 were highly activated and likely central to the oyster's antiviral response. Genes related to anti-apoptosis, oxidation, RNA and protein destruction were also highly up-regulated, while genes related to anti-oxidation were down-regulated. The oxidative burst induced by the up-regulation of oxidases and severe down-regulation of anti-oxidant genes may be important for the destruction of viral components, but may also exacerbate oyster mortality. This study provides unprecedented insights into antiviral response in a mollusc. The mobilization and complex regulation of expanded innate immune-gene families highlights the oyster genome's adaptation to a virus-rich marine environment. Article in Journal/Newspaper Crassostrea gigas HAL Sorbonne Université Fish & Shellfish Immunology 46 1 131 144
institution Open Polar
collection HAL Sorbonne Université
op_collection_id ftsorbonneuniv
language English
topic Marine virus
Ostreid herpesvirus OsHV-1μVar
Immune receptors
Antiviral response
Innate immunity
Viral RNA
Oyster
Oxidative burst
[SDV]Life Sciences [q-bio]
spellingShingle Marine virus
Ostreid herpesvirus OsHV-1μVar
Immune receptors
Antiviral response
Innate immunity
Viral RNA
Oyster
Oxidative burst
[SDV]Life Sciences [q-bio]
He, Yan
Jouaux, Aude
Ford, Susan, E.
Lelong, Christophe
Sourdaine, Pascal
Mathieu, Michel
Guo, Ximing
Transcriptome analysis reveals strong and complex antiviral response in a mollusc
topic_facet Marine virus
Ostreid herpesvirus OsHV-1μVar
Immune receptors
Antiviral response
Innate immunity
Viral RNA
Oyster
Oxidative burst
[SDV]Life Sciences [q-bio]
description International audience Viruses are highly abundant in the oceans, and how filter-feeding molluscs without adaptive immunity defend themselves against viruses is not well understood. We studied the response of a mollusc Crassostrea gigas to Ostreid herpesvirus 1 µVar (OsHV-1μVar) infections using transcriptome sequencing. OsHV-1μVar can replicate extremely rapidly after challenge of C. gigas as evidenced by explosive viral transcription and DNA synthesis, which peaked at 24 and 48 h post-inoculation, respectively, accompanied by heavy oyster mortalities. At 120 h post-injection, however, viral gene transcription and DNA load, and oyster mortality, were greatly reduced indicating an end of active infections and effective control of viral replication in surviving oysters. Transcriptome analysis of the host revealed strong and complex responses involving the activation of all major innate immune pathways that are equipped with expanded and often novel receptors and adaptors. Novel Toll-like receptor (TLR) and MyD88-like genes lacking essential domains were highly up-regulated in the oyster, possibly interfering with TLR signal transduction. RIG-1/MDA5 receptors for viral RNA, interferon-regulatory factors, tissue necrosis factors and interleukin-17 were highly activated and likely central to the oyster's antiviral response. Genes related to anti-apoptosis, oxidation, RNA and protein destruction were also highly up-regulated, while genes related to anti-oxidation were down-regulated. The oxidative burst induced by the up-regulation of oxidases and severe down-regulation of anti-oxidant genes may be important for the destruction of viral components, but may also exacerbate oyster mortality. This study provides unprecedented insights into antiviral response in a mollusc. The mobilization and complex regulation of expanded innate immune-gene families highlights the oyster genome's adaptation to a virus-rich marine environment.
author2 Ocean University of China (OUC)
Rutgers University System (Rutgers)
Biologie des Organismes et Ecosystèmes Aquatiques (BOREA)
Université de Caen Normandie (UNICAEN)
Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)
format Article in Journal/Newspaper
author He, Yan
Jouaux, Aude
Ford, Susan, E.
Lelong, Christophe
Sourdaine, Pascal
Mathieu, Michel
Guo, Ximing
author_facet He, Yan
Jouaux, Aude
Ford, Susan, E.
Lelong, Christophe
Sourdaine, Pascal
Mathieu, Michel
Guo, Ximing
author_sort He, Yan
title Transcriptome analysis reveals strong and complex antiviral response in a mollusc
title_short Transcriptome analysis reveals strong and complex antiviral response in a mollusc
title_full Transcriptome analysis reveals strong and complex antiviral response in a mollusc
title_fullStr Transcriptome analysis reveals strong and complex antiviral response in a mollusc
title_full_unstemmed Transcriptome analysis reveals strong and complex antiviral response in a mollusc
title_sort transcriptome analysis reveals strong and complex antiviral response in a mollusc
publisher HAL CCSD
publishDate 2015
url https://normandie-univ.hal.science/hal-02296483
https://doi.org/10.1016/j.fsi.2015.05.023
genre Crassostrea gigas
genre_facet Crassostrea gigas
op_source ISSN: 1050-4648
EISSN: 1095-9947
Fish and Shellfish Immunology
https://normandie-univ.hal.science/hal-02296483
Fish and Shellfish Immunology, 2015, 46 (1), pp.131-144. ⟨10.1016/j.fsi.2015.05.023⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1016/j.fsi.2015.05.023
hal-02296483
https://normandie-univ.hal.science/hal-02296483
doi:10.1016/j.fsi.2015.05.023
op_doi https://doi.org/10.1016/j.fsi.2015.05.023
container_title Fish & Shellfish Immunology
container_volume 46
container_issue 1
container_start_page 131
op_container_end_page 144
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