Doubling of the known set of RNA viruses by metagenomic analysis of an aquatic virome

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.

An Unconventional Flavivirus and Other RNA Viruses in the Sea Cucumber (Holothuroidea; Echinodermata) Virome

“…Picornavirus-like genomes are routinely recovered in invertebrate host-associated and environmental RNA viral metaviromes [ 12 , 33 , 61 , 62 , 63 , 64 , 65 , 66 , 67 , 68 ]. There have been no previous reports of picornaviruses associated with any disease in aquatic invertebrates, and their pattern of association between sea star wasting (SSW)-affected and grossly normal asteroid specimens does not suggest their involvement in disease process [ 33 ].…”

“…Phylogenetic analyses of detected Picornavirales based around the rhv domain demonstrate that they are similar to picorna-like viruses retrieved from transcriptomes of insects, suggesting an invertebrate host (Figure 4). Picornavirus-like genomes are routinely recovered in invertebrate host-associated and environmental RNA viral metaviromes [12,33,[61][62][63][64][65][66][67][68]. There have been no previous reports of picornaviruses associated with any disease in aquatic invertebrates, and their pattern of association between sea star wasting (SSW)-affected and grossly normal asteroid specimens does not suggest their involvement in disease process [33].…”

Viral discovery in the ‘realm’ of COVID‐19

“…Congruently, giant/jumbo bacteriophage with genomes >500 kb, virions longer than 600 nm, tRNA synthetases and proteinaceous nucleus‐like compartments posit exciting new questions about virion architectures, infection and defence strategies, and evolutionary trajectories (Malone et al ., 2020). Highlighting the utility of database mining, another study identified 10 000 RdRp genes, hallmarks of RNA viruses, prompting reevaluation of gene exchange between RNA viral families and complete reconstruction of the new ‘realm’ of the Ribovaria (Koonin 2020 ; Wolf et al ., 2020). Members of these newly discovered RNA viruses disproportionately infect invertebrates (Wolf et al ., 2020), plants (Dolja et al ., 2020), and metazoans (Koonin et al ., 2020), yet it remains unclear what impact that these fast‐evolving genomes have on their hosts.…”

VirION2: a short- and long-read sequencing and informatics workflow to study the genomic diversity of viruses in nature

“…Because most viruses are uncultivated, advances have mainly arisen through metagenomic approaches, which have rapidly improved with new sequencing technologies (Brum & Sullivan, 2015). The importance of viruses in community composition and nutrient cycling is also increasingly being recognized across diverse ecosystems, including soils (Emerson et al, 2018; Trubl et al, 2018), the human microbiome (Shkoporov et al, 2019), glacial ice (Zhong et al, 2020), and invertebrates (Shi et al, 2016; Wolf et al, 2020). For example, viruses have the potential to aid in soil carbon flux by encoding plant polysaccharide-degrading enzymes (Emerson et al, 2018), or can be involved in human gut dysbiosis that leads to various health issues (Mirzaei & Maurice, 2017).…”