Abstract
Sea cucumbers (Holothuroidea; Echinodermata) are ecologically significant constituents of benthic marine habitats. We surveilled RNA viruses inhabiting eight species (representing four families) of holothurian collected from four geographically distinct locations by viral metagenomics, including a single specimen of Apostichopus californicus affected by a hitherto undocumented wasting disease. The RNA virome comprised genome fragments of both single-stranded positive sense and double stranded RNA viruses, including those assigned to the Picornavirales, Ghabrivirales, and Amarillovirales. We discovered an unconventional flavivirus genome fragment which was most similar to a shark virus. Ghabivirales-like genome fragments were most similar to fungal totiviruses in both genome architecture and homology and had likely infected mycobiome constituents. Picornavirales, which are commonly retrieved in host-associated viral metagenomes, were similar to invertebrate transcriptome-derived picorna-like viruses. The greatest number of viral genome fragments was recovered from the wasting A. californicus library compared to the asymptomatic A. californicus library. However, reads from the asymptomatic library recruited to nearly all recovered wasting genome fragments, suggesting that they were present but not well represented in the grossly normal specimen. These results expand the known host range of flaviviruses and suggest that fungi and their viruses may play a role in holothurian ecology.
Highlights
Generation DNA sequencing technology applied to viral metagenomics has enabled surveillance of viruses associated with invertebrate tissues
We found that viruses associated with these tissues were dominated by Picornavirales (Marnaviridae) and Ghabrivirales (Totiviridae), but report on the presence of a deeply branched flavivirus in two holothurian species in the northeast Pacific Ocean
To the best of our knowledge, this is the first viral metagenomic survey of holothurians, and our work expands on knowledge of viruses inhabiting echinoderms
Summary
Generation DNA sequencing technology applied to viral metagenomics has enabled surveillance of viruses associated with invertebrate tissues. These studies, along with the mining of metazoan transcriptomes, have led to the discovery of novel viral lineages in aquatic invertebrates and broadened the host range of several viral families [1,2,3,4,5,6,7,8,9,10,11,12,13,14,15]. Study of novel and/or highly divergent viral genomes across a wider range of aquatic invertebrates may provide clues to viral evolution and potential roles in host ecology. Holothurians (Holothuroidea; Echinodermata) are ecologically important echinoderms [17,18]
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