Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas

Maxime Lafont,Bruno Petton,Agnès Vergnes,Benjamin Gourbal,Marianna Pauletto,Caroline Montagnani,Amélie Segarra

doi:10.1038/s41598-017-13564-0

Abstract

In the last decade, a paradigm shift has emerged in comparative immunology. Invertebrates can no longer be considered to be devoid of specific recognition and immune memory. However, we still lack a comprehensive view of these phenomena and their molecular mechanisms across phyla, especially in terms of duration, specificity, and efficiency in a natural context. In this study, we focused on a Lophotrochozoan/virus interaction, as antiviral priming is mostly overlooked in molluscs. Juvenile Crassostrea gigas oysters experience reoccurring mass mortalities events from Ostreid herpes virus 1 with no existing therapeutic treatment. Our results showed that various nucleic acid injections can prime oysters to trigger an antiviral state ultimately protecting them against a subsequent viral infection. Focusing on poly(I:C) as elicitor, we evidenced that it protected from an environmental infection, by mitigating viral replication. That protection seemed to induce a specific antiviral response as poly(I:C) fails to protect against a pathogenic bacteria. Finally, we showed that this phenomenon was long-lasting, persisting for at least 5 months thus suggesting for the first time the existence of innate immune memory in this invertebrate species. This study strengthens the emerging hypotheses about the broad conservation of innate immune priming and memory mechanisms in Lophotrochozoans.

Highlights

Studies testing this phenomenon in invertebrates appear to be quite heterogeneous and largely differ in terms of experimental design, host-parasite combinations, elicitors used for priming
We still lack a comprehensive view of the antiviral immune priming phenomenon in the oyster. It is unknown whether the different double stranded RNA (dsRNA) or other nucleic acids are efficient to prime oysters; if poly(I:C) is able to reduce mortalities as well as viral loads; if the protection can extend over 54 h of priming; if that protection is restricted to antiviral response and if it is efficient in the environment
We tested the poly(I:C) HMW previously used, poly(I:C) of low molecular weight (LMW), in-house synthesized double- or single-stranded RNA derived from the gene encoding the green fluorescent protein (GFP) or from the ORF 87 of the OsHV-1 encoding an inhibitor of apoptosis

Summary

Introduction

Studies testing this phenomenon in invertebrates appear to be quite heterogeneous and largely differ in terms of experimental design, host-parasite combinations, elicitors used for priming Previous studies showed that HMW poly(I:C) and dsRNA were able to significantly reduce viral loads upon OsHV-1 infection and mortality rates regarding dsRNA priming.

Results

Conclusion