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As filter-feeding bivalves, mussels have been traditionally studied as possible vectors of different bacterial or viral pathogens. The absence of a known viral pathogen in these bivalves makes it particularly interesting to study the interaction of the mussel innate immune system with a virus of interest. In the present work, mussels were challenged with viral haemorrhagic septicaemia virus (VHSV), which is a pathogen in several fish species. The viral load was eliminated after 24 h and mussels evidenced antiviral activity towards VHSV, demonstrating that the virus was recognized and eliminated by the immune system of the host and confirming that mussels are not VHSV vectors in the marine environment. The transcriptome activating the antiviral response was studied, revealing the involvement of cytoplasmic viral sensors with the subsequent activation of the JAK-STAT pathway and several downstream antiviral effectors. The inflammatory response was inhibited with the profound downregulation of MyD88, shifting the immune balance towards antiviral functions. High modulation of retrotransposon activity was observed, revealing a mechanism that facilitates the antiviral response and that had not been previously observed in these species. The expression of several inhibitors of apoptosis and apoptosis-promoting genes was modulated, although clear inhibition of apoptosis in bivalves after severe viral infection and subsequent disease was not observed in this study. Finally, the modulated expression of several long noncoding RNAs that were correlated with genes involved in the immune response was detected. • VHSV does not replicate and it is eliminated after being incorporated by mussels. • Mussel immune response follows antiviral pathways conserved in metazoans. • Upon viral recognition, antiviral signaling leads to JAK/STAT effector response. • MyD88 inflammatory pathway is inhibited in favor of the antiviral response. • Retrotransposons and apoptosis regulators are implicated in the antiviral response. [ABSTRACT FROM AUTHOR]