A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas

Over the last decade, innate immune priming has been evidenced in many invertebrate phyla. If mechanistic models have been proposed, molecular studies aiming to substantiate these models have remained scarce. We reveal here the transcriptional signature associated with immune priming in the oyster Crassostrea gigas. Oysters were fully protected against Ostreid herpesvirus 1 (OsHV-1), a major oyster pathogen, after priming with poly(I·C), which mimics viral double-stranded RNA. Global analysis through RNA sequencing of oyster and viral genes after immune priming and viral infection revealed that poly(I·C) induces a strong antiviral response that impairs OsHV-1 replication. Protection is based on a sustained upregulation of immune genes, notably genes involved in the interferon pathway and apoptosis, which control subsequent viral infection. This persistent antiviral alert state remains active over 4 months and supports antiviral protection in the long term. This acquired resistance mechanism reinforces the molecular foundations of the sustained response model of immune priming. It further opens the way to applications (pseudovaccination) to cope with a recurrent disease that causes dramatic economic losses in the shellfish farming industry worldwide.

Keyword(s)

innate immunity, priming, OsHV-1, antiviral response, immune memory, oyster, POMS, poly(I-C), interferon, transcriptomic

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173 Mo
TABLE S1 Library and mapped reads on the C. gigas genome or OsHV-1 genome used for RNA-seq analyses.
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FIG S1 Technical validation of the RNA-seq data by RT-qPCR. Twenty genes with contrasting expression levels were selected...
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FIG S2 Distribution of differentially expressed genes postpriming. Numbers of DEG following poly(I·C) injection upregulated (red) or downregulated (green) are plotted following their fold change leve
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TABLE S2 Primers used for RNA-seq validation and RT-qPCR analyses.
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TABLE S3 (A) List of differentially expressed genes postpriming with poly(I·C); (B) DEG identification in primed oysters postchallenge.
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FIG S3 Hierarchical clustering trees of Gene ontology categories affected by poly(I·C) priming. Hierarchical clustering trees of significant GO categories belonging to biological processes ...
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TABLE S4 List of enriched categories identified by RBGOA
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TABLE S5 (A) List of the 1,587 DEG regulated postpriming and their respective genome identifier, annotation, GO correspondence and FC, and RPKM in postpriming and postchallenge ...
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FIG S4 Comparative analysis of the poly(I·C) sustained expression pattern and the FSW-specific challenge. (A) Venn diagram representing the genes common to the two patterns. (B) Comparison of the...
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FIG S5 Experimental design used to identify the long-term molecular basis underlying poly(I·C) priming. (A) Specific-pathogen-free (SPF) oysters, highly susceptible to juvenile oyster syndrome, ...
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How to cite
Lafont Maxime, Vergnes Agnes, Vidal-Dupiol Jeremie, de Lorgeril Julien, Gueguen Yannick, Haffner Philippe, Petton Bruno, Chaparro Cristian, Barrachina Celia, Destoumieux-Garzon Delphine, Mitta Guillaume, Gourbal Benjamin, Montagnani Caroline (2020). A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas. Mbio. 11 (2). e02777-19 (17p.). https://doi.org/10.1128/mBio.02777-19, https://archimer.ifremer.fr/doc/00614/72580/

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