A comprehensive RNA virome identified in the oyster Magallana gigas reveals the intricate network of virus sharing between seawater and mollusks

Abstract Background As a globally farmed oyster species, Magallana gigas has garnered significant attention due to the contaminated RNA viruses that have caused illness in humans. However, limited knowledge is available on the bioaccumulation status and overall diversity of RNA virome in the M. gigas digestive tissues (DTs). Moreover, there is a lack of understanding regarding the shared community of RNA virome among intertidal mollusks. To address these knowledge gaps, we performed a comprehensive meta-transcriptomic analysis of 173 M . gigas samples from the East China Sea and compared the viral sequences to the meta-transcriptomes of other mollusks and seawater (i.e., the oyster Magallana hongkongensis, bivalves, gastropods, cephalopods, and Yangshan Harbor) through RdRP identification and reads mapping. Results Our results indicate that 154 viral RdRPs were confidently identified in the M. gigas DT, with 94% (144/154) showing less than 90% amino acid identity. This indicates the presence of at least 144 putative novel RNA virus species in M. gigas DT. All viruses belonged to the phyla Lenarviricota, Pisuviricota, and Kitrinoviricota, and the marna-like viruses constituted the most diverse assemblage among these newly identified viruses. Furthermore, members of marna-like, picobirna-like, and noda-like virus groups comprise the most prevalent viruses in the M. gigas meta-transcriptome, with 14 RdRP-bearing sequences accounting for at least 1% of the overall aligned reads. M. hongkongensis has been found to harbor the most diverse viruses found in M. gigas, while 37 and 25 newly identified RNA viruses in oysters were discovered in an octopus meta-transcriptome and seawater virome, respectively. Conclusions The findings provide insights into the cryptic and hitherto unstudied virus-sharing network across the marine food web. Moreover, the viruses identified in oysters have the potential to serve as indicators for identifying the circulation of marine RNA viruses. Video Abstract