A comprehensive RNA virome from molluscan transcriptomes reveals extensive diversity and modular genome evolution

Mollusca is the second-largest animal phylum and an important marine food resource for humans. While DNA viruses that threaten molluscan aquaculture have received much attention, molluscan RNA viromes remain poorly explored. Here, based on 223 molluscan metatranscriptomes covering eight animal classes, we identified 80 species-level RNA viruses spanning three viral phyla and nine viral families. Phylogenetic result combined structural modeling found a major increase in the number of Pisuviricota-related lineages. Extensive modular evolution in viral genomes was observed including gene rearrangements and co-evolution of capsid and RdRP genes. Host prediction linked 78% of the RNA viruses to a diverse range of eukaryotes, including vertebrates, invertebrates, and algae. These findings expand the known diversity of RNA viruses in molluscs and shed light on their phylogenetic relationships, highlighting molluscs as valuable models for RNA virus evolution. Graphical abstractRNA virus diversity within 223 molluscan transcriptome samples were analyzed based on RdRP identification. Viruses belonging to the phylum Pisoviricota were the most abundant; co-evolution between RdRP and capsid proteins of molluscan Picornavirales was revealed, and a complex virus-host interaction network was constructed. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=153 SRC="FIGDIR/small/673676v1_ufig1.gif" ALT="Figure 1"> View larger version (44K): org.highwire.dtl.DTLVardef@1ce8fc0org.highwire.dtl.DTLVardef@3f9068org.highwire.dtl.DTLVardef@121cc2forg.highwire.dtl.DTLVardef@1e431a0_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LIComprehensive metatranscriptomic analysis found extensive RNA viral diversity in molluscs. C_LIO_LIPisuviricota dominate the molluscan RNA virome, substantially broadening known viral lineages. C_LIO_LIModular genome evolution involving gene rearrangements and conserved structural features characterize molluscan RNA viruses. C_LIO_LIMolluscs potentially serve as major ecological reservoirs for diverse RNA viruses infecting various eukaryotic hosts. C_LI