Viromes in marine ecosystems reveal remarkable invertebrate RNA virus diversity

Abstract

Ocean viromes remain poorly understood and little is known about the ecological factors driving aquatic RNA virus evolution. In this study, we used a meta-transcriptomic approach to characterize the viromes of 58 marine invertebrate species across three seas. This revealed the presence of 315 newly identified RNA viruses in nine viral families or orders (Durnavirales, Totiviridae, Bunyavirales, Hantaviridae, Picornavirales, Flaviviridae, Hepelivirales, Solemoviridae and Tombusviridae), with most of them are sufficiently divergent to the documented viruses. With special notice that we first time revealed an ocean virus rooting to mammalian hantaviruses. We also found evidence for possible host sharing and switch events during virus evolution. In sum, we demonstrated the hidden diversity of marine invertebrate RNA viruses.

The RNA Virome of Echinoderms

“…The majority of the echinoderm-associated picornaviruses grouped into the Dicistroviridae, Iflaviridae , and Marnaviridae families, but other recovered viruses also comprised novel clades (Figure 3) which supported our expectation that the extant diversity of echinoderm RNA viruses is under sampled. The Marnaviridae are known to be ocean virioplankton which infect single-celled eukaryotes, such as phytoplankton and protists, but have also been found from metatranscriptomes from marine bivalves [48, 49]. It is possible that the Marnaviridae we observed infect protists that are symbionts or transiently associated with echinoderms.…”

“…The most prevalent RNA viruses in echinoderm transcriptomes and RNA viral metagenomes were picornaviruses which are non-enveloped, single-stranded RNA (+ssRNA) viruses. The order Picornavirales is comprised of eight families ( Caliciviridae, Dicistroviridae, Iflaviridae, Marnaviridae, Picornaviridae, Polycipiviridae, Secoviridae , and Solinviviridae ) and 103 genera and are among the most prevalent and diverse group of viruses found in -omics surveys of animal and environmental samples [47, 29, 38, 48]. The majority of the echinoderm-associated picornaviruses grouped into the Dicistroviridae, Iflaviridae , and Marnaviridae families, but other recovered viruses also comprised novel clades (Figure 3) which supported our expectation that the extant diversity of echinoderm RNA viruses is under sampled.…”

“…The host range of many viral groups has changed considerably in recent years, and there are examples of host ranges within RNA viral families that do extend from protists to mammals, such as Reoviridae [50, 51]. All classified species of Dicistroviridae and Iflaviridae infect arthropods, and have largely been characterized due to the economic impacts of their pathogenicity though the host range of these families likely extends far beyond arthropods given their presence in metatranscriptomes from organisms in the phyla Mollusca, Cnidaria, and Platyhelminthes [31, 48, 52]. The disease severity from infections of both families ranges from inapparent to lethal, supporting the possibility that there may be non-pathogenic species infecting echinoderms.…”

“…The vast majority of viruses recovered here, and elsewhere, using transcriptomic and metatranscriptomic approaches have been positive-sense single-stranded RNA (+ssRNA) [1, 48, 53]. This pattern of abundance likely has a basis in biology, but in the case of our dataset, may be inflated due to our use of transcriptomic data.…”

“…The selection for polyadenylated transcripts during RNA-seq library preparation biases towards +ssRNA viruses, like picornaviruses, which have 3’polyadenylated tails [54, 55]. Studies utilizing a metatranscriptomic approach for RNA viral discovery generally do not find such a highly skewed distribution towards +ssRNA but are nevertheless the most abundant viral type [1, 29, 38, 48]. By utilizing viral RNA metagenomes and transcriptomes we have uncovered the fullest diversity of RNA viruses associated with echinoderms with the datasets available, though we expect future multi-omic efforts to reveal additional diversity.…”