Abstract
RNA viruses in aquatic environments remain poorly studied. Here, we analysed the RNA virome from approximately 10 l water from Yangshan Deep-Water Harbour near the Yangtze River estuary in China and identified more than 4,500 distinct RNA viruses, doubling the previously known set of viruses. Phylogenomic analysis identified several major lineages, roughly, at the taxonomic ranks of class, order and family. The 719-member-strong Yangshan virus assemblage is the sister clade to the expansive class Alsuviricetes and consists of viruses with simple genomes that typically encode only RNA-dependent RNA polymerase (RdRP), capping enzyme and capsid protein. Several clades within the Yangshan assemblage independently evolved domain permutation in the RdRP. Another previously unknown clade shares ancestry with Potyviridae, the largest known plant virus family. The ‘Aquatic picorna-like viruses/Marnaviridae’ clade was greatly expanded, with more than 800 added viruses. Several RdRP-linked protein domains not previously detected in any RNA viruses were identified, such as the small ubiquitin-like modifier (SUMO) domain, phospholipase A2 and PrsW-family protease domain. Multiple viruses utilize alternative genetic codes implying protist (especially ciliate) hosts. The results reveal a vast RNA virome that includes many previously unknown groups. However, phylogenetic analysis of the RdRPs supports the previously established five-branch structure of the RNA virus evolutionary tree, with no additional phyla.
Highlights
Metagenomics and metaviromics have led to rapid progress in virus discovery[1,2,3,4,5,6,7,8,9]
RNA virome analysis performed using complementary DNA derived from approximately 10 l of samples from Yangshan Deep-Water Harbour yielded 4,593 nearly full-length RNA virus RNA-dependent RNA polymerase (RdRP) that formed 2,192 clusters at 75% amino acid identity which represents virus diversity at a level between species and genus
Phylogenetic analysis assigned 85% of the RdRPs from the Yangshan RNA virome to 9 clades and one complex assemblage, each comprising more than 100 RdRps from several clusters (Fig. 2 and Supplementary Dataset 1)
Summary
Metagenomics and metaviromics (that is, sequencing of DNA or RNA from virus particle fractions isolated from diverse environments or organisms) have led to rapid progress in virus discovery[1,2,3,4,5,6,7,8,9]. Perhaps the best characterized group of such viruses is the family Marnaviridae, which combines picorna-like viruses of diatoms and other stramenopiles[21,22,23,24,25,26] with a growing number of species defined by metagenomics as probably infecting related aquatic unicellular eukaryotes[27,28] (hereafter referred to as ‘protists’). Another key development has been meta-transcriptome sequencing of invertebrate holobionts, doubling the size of the known RNA virome[29,30,31,32,33]. A pressing question remains: would the Nature Microbiology | VOL 5 | October 2020 | 1262–1270 | www.nature.com/naturemicrobiology
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