Abstract
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.IMPORTANCE In the last decade, important discoveries have shown that resistance to reinfection can be achieved without a functional adaptive immune system, introducing the concept of innate immune memory in invertebrates. However, this field has been constrained by the limited number of molecular mechanisms evidenced to support these phenomena. Taking advantage of an invertebrate species, the Pacific oyster (Crassostrea gigas), in which we evidenced one of the longest and most effective periods of protection against viral infection observed in an invertebrate, we provide the first comprehensive transcriptomic analysis of antiviral innate immune priming. We show that priming with poly(I·C) induced a massive upregulation of immune-related genes, which control subsequent viral infection, and it was maintained for over 4 months after priming. This acquired resistant mechanism reinforces the molecular foundations of the sustained response model of immune priming. It opens the way to pseudovaccination to prevent the recurrent diseases that currently afflict economically or ecologically important invertebrates.
Highlights
Over the last decade, innate immune priming has been evidenced in many invertebrate phyla
To characterize the molecular foundations underlying innate immune priming in the oyster, we used a biparental oyster family highly susceptible to Pacific oyster juvenile oyster syndrome (POMS) [14]
F11 oysters were primed with poly(I·C) and experimentally challenged with Ostreid herpesvirus 1 (OsHV-1) 10 days postpriming (DPP)
Summary
Innate immune priming has been evidenced in many invertebrate phyla. 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. We show that priming with poly(I·C) induced a massive upregulation of immune-related genes, which control subsequent viral infection, and it was maintained for over 4 months after priming This acquired resistant mechanism reinforces the molecular foundations of the sustained response model of immune priming. Reports have suggested the implication of certain classes of multigene family receptors (Down syndrome cell adhesion molecules [DSCAMS] and fibrinogen-related proteins [FREPs]) and immune effectors (antimicrobial peptides) and cellular processes (phagocytosis and hematopoietic proliferation) in immune priming [6,7,8,9,10,11] In spite of these scattered data, a key question still pending is that of the molecular foundations supporting these mechanistic models [12]
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