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...
Published in: | Fish & Shellfish Immunology |
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Online Access: | https://hal-normandie-univ.archives-ouvertes.fr/hal-02296483 https://doi.org/10.1016/j.fsi.2015.05.023 |
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ftccsdartic:oai:HAL:hal-02296483v1 2023-05-15T15:59:02+02:00 Transcriptome analysis reveals strong and complex antiviral response in a mollusc He, Yan Jouaux, Aude Ford, Susan, 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://hal-normandie-univ.archives-ouvertes.fr/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://hal-normandie-univ.archives-ouvertes.fr/hal-02296483 doi:10.1016/j.fsi.2015.05.023 ISSN: 1050-4648 EISSN: 1095-9947 Fish and Shellfish Immunology https://hal-normandie-univ.archives-ouvertes.fr/hal-02296483 Fish and Shellfish Immunology, Elsevier, 2015, 46 (1), pp.131-144. ⟨10.1016/j.fsi.2015.05.023⟩ Marine virus Ostreid herpesvirus OsHV-1μVar Innate immunity Antiviral response Immune receptors Viral RNA Oxidative burst Oyster [SDV]Life Sciences [q-bio] info:eu-repo/semantics/article Journal articles 2015 ftccsdartic https://doi.org/10.1016/j.fsi.2015.05.023 2021-12-05T02:01:11Z 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 Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Fish & Shellfish Immunology 46 1 131 144 |
institution |
Open Polar |
collection |
Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) |
op_collection_id |
ftccsdartic |
language |
English |
topic |
Marine virus Ostreid herpesvirus OsHV-1μVar Innate immunity Antiviral response Immune receptors Viral RNA Oxidative burst Oyster [SDV]Life Sciences [q-bio] |
spellingShingle |
Marine virus Ostreid herpesvirus OsHV-1μVar Innate immunity Antiviral response Immune receptors Viral RNA Oxidative burst Oyster [SDV]Life Sciences [q-bio] He, Yan Jouaux, Aude Ford, Susan, 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 Innate immunity Antiviral response Immune receptors Viral RNA Oxidative burst Oyster [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, Lelong, Christophe Sourdaine, Pascal Mathieu, Michel Guo, Ximing |
author_facet |
He, Yan Jouaux, Aude Ford, Susan, 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://hal-normandie-univ.archives-ouvertes.fr/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://hal-normandie-univ.archives-ouvertes.fr/hal-02296483 Fish and Shellfish Immunology, Elsevier, 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://hal-normandie-univ.archives-ouvertes.fr/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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1766394820279926784 |