Eukaryotic Microbial RNA Viruses-Acute or Persistent? Insights into Their Function in the Aquatic Ecosystem

Abstract

Isolated RNA viruses mainly parasitize eukaryotes. RNA viruses either expand horizontally by infecting hosts (acute type) or coexist with the host and are vertically inherited (persistent type). The significance of persistent-type RNA viruses in environmental viromes (the main hosts are expected to be microbes) was only recently reported because they had previously been overlooked in virology. In this review, we summarize the host-virus relationships of eukaryotic microbial RNA viruses. Picornavirales and Reoviridae are recognized as representative acute-type virus families, and most of the microbial viruses in Narnaviridae, Totiviridae, and Partitiviridae are categorized as representative persistent-type viruses. Acute-type viruses have only been found in aquatic environments, while persistent-type viruses are present in various environments, including aquatic environments. Moreover, persistent-type viruses are potentially widely spread in the RNA viral sequence space. This emerging evidence provides novel insights into RNA viral diversity, host-virus relationships, and their history of co-evolution.

Keywords: RNA virus; aquatic; eukaryote.

Fig. 1.

Schematic of transmission routes of microbial RNA viruses.

Fig. 2.

A total of 293 isolated acute- and persistent-type microbial RNA viruses in sequence-based clusters. Colored circles indicate the lifestyle of each RNA virus: red, acute; blue, persistent. In total, 315 isolated microbial eukaryotic RNA viruses were collected from the manually curated Virus-Host database (Mihara et al., 2016) downloaded on 2021.12.09. Sequences were clustered at 70% amino acid identity. Representative sequences were applied to a network ana­lysis with MOCASSIN-prot (Keel et al., 2018).

Fig. 3.

RdRp sequences of known RNA viruses obtained from the Identical Protein Groups resource (https://www.ncbi.nlm.nih.gov/ipg) with keywords “rna dependent rna polymerase” and “viruses”. After the removal of short (<200 aa) sequences, RdRp sequences were clustered at 70% using CD-HIT (Huang et al., 2010). Representative sequences were applied to a network ana­lysis with MOCASSIN-prot (Keel et al., 2018). Colored circles indicate percent identity to persistent- or acute-type microbial RNA viruses: blue 100% to persistent; sky blue >70% to persistent; green >50% to persistent; red 100% to acute (>70 and 50% to acute were not identified).

Fig. 4.

Differences in conventional RNA-seq and FLDS for resultant contigs. In a de novo ana­lysis, terminal sequence positions were not defined by RNA-seq data. However, FLDS data enabled us to identify terminal sequence positions because FLDS sequence reads included RACE (Rapid Amplification of cDNA Ends), which is widely used to assess the terminal sequences of RNA molecules (Urayama et al., 2016).

Fig. 5.

Concept of RNA viral genome reconstruction based on conserved terminal sequences in segmented RNA virus genomes. Many segmented RNA viruses have conserved 5′- and 3′-terminal sequences (colored boxes). FLDS enabled us to obtain full-length RNA sequences, which are difficult to obtain with conventional RNA-seq technologies (Fig. 2). Based on terminal sequences, we reconstructed RNA viral genomes. If RdRp is identified in a potential RNA viral genome, we predict that other RNA sequences, which do not show significant similarity to known RNA viruses, will be segments of the RNA virus.