Metagenomics reshapes the concepts of RNA virus evolution by revealing extensive horizontal virus transfer

Abstract

Virus metagenomics is a young research filed but it has already transformed our understanding of virus diversity and evolution, and illuminated at a new level the connections between virus evolution and the evolution and ecology of the hosts. In this review article, we examine the new picture of the evolution of RNA viruses, the dominant component of the eukaryotic virome, that is emerging from metagenomic data analysis. The major expansion of many groups of RNA viruses through metagenomics allowed the construction of substantially improved phylogenetic trees for the conserved virus genes, primarily, the RNA-dependent RNA polymerases (RdRp). In particular, a new superfamily of widespread, small positive-strand RNA viruses was delineated that unites tombus-like and noda-like viruses. Comparison of the genome architectures of RNA viruses discovered by metagenomics and by traditional methods reveals an extent of gene module shuffling among diverse virus genomes that far exceeds the previous appreciation of this evolutionary phenomenon. Most dramatically, inclusion of the metagenomic data in phylogenetic analyses of the RdRp resulted in the identification of numerous, strongly supported groups that encompass RNA viruses from diverse hosts including different groups of protists, animals and plants. Notwithstanding potential caveats, in particular, incomplete and uneven sampling of eukaryotic taxa, these highly unexpected findings reveal horizontal virus transfer (HVT) between diverse hosts as the central aspect of RNA virus evolution. The vast and diverse virome of invertebrates, particularly nematodes and arthropods, appears to be the reservoir, from which the viromes of plants and vertebrates evolved via multiple HVT events.

Keywords: Horizontal virus transfer; Metaviromics; RNA viruses; Virus evolution; Virus metagenomics.

Fig. 1

Evolution of the narnavirus-like (+)RNA viruses. (A) Schematic dendrogram based on the phylogenetic tree for RNA-dependent RNA polymerases (RdRp) of Narna-Levi clade from Shi et al. (2016a). Major clusters of related viruses are shown as triangles colored in accord with virus host ranges: grey, bacteria; olive, fungi; blue, invertebrates; green, plants. Rough diagrams of typical virus genomes for each cluster showing encoded proteins (rectangles; homologous proteins are in the same color), their functions and the genome size in kilobases (Kb), are at the right. CP, capsid protein; MP, movement protein; S3H, superfamily 3 helicase. (B) Hypothetical scenario for the evolution of narnavirus-like viruses. Vertical arrows denote virus transmission that accompanies host evolution, whereas horizontal arrows show presumed horizontal virus transfer (HVT) between distinct host organisms.

Fig. 2

Evolution of the picorna-like (+)RNA viruses. (A) Schematic dendrogram based on phylogenetic tree for RNA-dependent RNA polymerases (RdRp) of the Picorna-Calici clade from Shi et al. (2016a). Major clusters of the related viruses are shown as triangles colored in accord with virus host ranges: red, vertebrates; blue, invertebrates; green, plants; plum, protists. Approximate diagrams of typical virus genomes for each cluster showing encoded proteins and their functions (rectangles; homologous proteins are in the same color) and the genome size in kilobases (Kb) are at the right. CP, capsid protein; MP, movement protein; Pro, protease; S3H, superfamily 3 helicase. (B) Hypothetical scenario for the evolution of picornavirus-like viruses. Vertical arrows denote virus transmission that follows host evolution, whereas horizontal arrows show presumed horizontal virus transfer (HVT) events between distinct host organisms.

Fig. 3

Evolution of the mononegavirus-like (−)RNA viruses. (A) Schematic dendrogram based on the phylogenetic tree for RNA-dependent RNA polymerases (RdRp) of the Mono-Chu clade from Shi et al. (2016a). Major clusters of the related viruses are shown as triangles colored in accord with the virus host ranges: blue, invertebrates; red, vertebrates; olive, fungi; green, plants (corresponds to arthropod-transmitted plant viruses); purple, insects and vertebrates. Rough diagrams of typical virus genomes for each cluster showing encoded proteins and their functions (rectangles; homologous proteins are in the same color) and the genome size in kilobases (Kb) are shown at the right. NC, nucleocapsid protein; M, matrix protein; P, phosphoproten; GP, glycoprotein; FGP, fusion glycoprotein; MP, movement protein; HAN, hemagglutinin-neuraminidase. (B) Hypothetical scenario for the evolution of (−)RNA viruses. Vertical arrows denote virus transmission that accompanies host evolution, whereas horizontal arrows show presumed horizontal virus transfer (HVT) events between distinct host organisms.

Fig. 4

Evolutionary relationships between viruses and their host organisms. The vertical and bended arrows denote major transitions in the evolution of the cellular organisms, whereas horizontal arrows show hypothetical events of horizontal virus transfer (HVT) from the viromes of the ancestral organisms to the newly evolving groups of organisms.