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Koonin and Dolja BMC Biology 2012, 10:54 http://www.biomedcentral.com/1741-7007/10/54 COMMENTARY Open Access Expanding networks of RNA virus evolution Eugene V Koonin*1 and Valerian V Dolja2 See research article: www.biomedcentral.com/1471-2148/12/91 unexpected evolutionary relationships have been revealed Abstract between viruses with different genomic strategies that In a recent BMC Evolutionary Biology article, Huiquan infect widely different hosts. A small set of virus hallmark Liu and colleagues report two new genomes of genes encoding proteins essential for virus replication double-stranded RNA (dsRNA) viruses from fungi and and morphogenesis form different combinations in use these as a springboard to perform an extensive diverse viruses but are absent from cellular genomes [2]. phylogenomic analysis of dsRNA viruses. The results Along with lineage­specific genes present in subsets of support the old scenario of polyphyletic origin of viruses, the hallmark genes account for a rich network of dsRNA viruses from different groups of positive-strand evolutionary connections against the background of the RNA viruses and additionally reveal extensive horizontal extreme diversity of viruses. In the last few years, new gene transfer between diverse viruses consistent with technologies, in particular the rapid progress of meta­ the network-like rather than tree-like mode of viral genomics (indiscriminate sequencing of environmental evolution. Together with the unexpected discoveries DNA samples), have revealed many surprising novelties of the first putative archaeal RNA virus and a RNA-DNA in the virus world. Perhaps the prime example is the virus hybrid, this work shows that RNA viral genomics discovery of giant viruses and their parasites, the viro­ has major surprises to deliver. phages [3]. However, unexpected findings with sub stan­ tial implications are also being reported for the much smaller and simpler RNA viruses. Commentary In a recent BMC Evolutionary Biology article, Huiquan Viruses are the most abundant and genetically diverse Liu and colleagues [4] report the genomes of two novel biological entities on earth as demonstrated by recent dsRNA viruses from fungi and proceed to place these metagenomic studies [1]. Unlike cellular life forms that viruses in the overall context of dsRNA virus evolution. all possess the same basic mechanism of genome repli­ dsRNA viruses have been isolated from animals, plants, cation and expression based upon double­stranded (ds) protists and bacteria but are particularly characteristic in DNA genome and positive­strand messenger (plus) RNA, fungi where they constitute the majority of the known viruses use all forms of genetic material (positive­strand, viruses. Some of the dsRNA viruses form typical virions negative­strand and dsRNA, single­stranded (ss)DNA, with genomes encased in a capsid whereas others are dsDNA) and execute virtually all conceivable genomic capsid­less, plasmid­like genetic elements. On the whole, strategies (RNA or DNA replication and transcription, as there is little doubt that dsRNA viruses make up a well as reverse transcription of RNA to DNA). In parti cu­ polyphyletic assemblage, with different members having lar, viruses with RNA genomes that do not go through a evolved from different lineages of positive­strand RNA DNA stage in their reproduction are the simplest genetic viruses on multiple, independent occasions [5]. For elements, reminiscent of the putative primordial RNA instance, three families of capsid­less dsRNA viruses that world. reproduce in fungi, plants or fungal mitochondria clearly Owing to their (relatively) small genomes and often originate from three distinct groups of positive­strand rapid reproduction, diverse viral genomes were charac­ RNA viruses: Hypoviridae infecting plant pathogenic ter ized in the early days of genomics, and many fungi from plant potyviruses [6]; Endornaviridae from alphavirus­like superfamily positive­strand RNA viruses of plants [7]; and fungal mitochondrial narnaviruses from *Correspondence: [email protected] 1National Center for Biotechnology Information, National Institutes of Health, bacterial positive­strand RNA viruses (Leviviridae) [8]. Bethesda, MD 20894, USA The origins of the rest of the dsRNA viruses are murkier, Full list of author information is available at the end of the article although the families Totiviridae and Partitiviridae have © 2012 Koonin and Dolja; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Koonin and Dolja BMC Biology 2012, 10:54 Page 2 of 4 http://www.biomedcentral.com/1741-7007/10/54 been tentatively linked to different groups of picorna­ proteins of plant viruses, most likely of the family Tombus­ virus­like positive­strand RNA viruses [6]. viridae [10]. Thus, in this case, a distinct group of viruses The only gene that is conserved in all dsRNA viruses evolved via reassortment of genomic segments derived along with positive­strand RNA viruses is the RNA­ from extremely diverse viruses, one of which is (at least dependent RNA polymerase (RdRp), and most of the nominally) a capsid­less dsRNA virus­like replicon conclusions on evolution of RNA viruses are based on whereas the other is a regular positive­strand RNA virus. RdRp phylogeny supplemented by phylogenies of other Metagenomics, a new major avenue of biological genes that are conserved in subsets of viruses and com­ discovery, delivers even more unexpected viral genome parative analysis of genome organization [6]. Huiquan arrangements. A recent metagenomic study of the virome Liu and colleagues [4] present the most complete of a geothermal lake in California revealed a small phylogeny so far of the RdRp for dsRNA viruses and circular genome that combines, within one ssDNA overlay the tree with the data on genome organization, segment, genes encoding a capsid protein clearly related virion structure and host range of the respective viruses. to that of plant positive­strand RNA tombusviruses and a The result is fascinating: several clades of RdRps en com­ rolling circle replication initiation endonuclease homolo­ pass viruses infecting diverse hosts (fungi, plants, protists gous to those of ssDNA circoviruses and nanoviruses and insects); viruses with and without capsids; and (Figure 1) [11]. This putative virus ­ in metagenomics the viruses with different numbers of genomic segments. As genome sequence comes before the organism or virus is long as the RdRp phylogeny is adopted as the scaffold for characterized ­ seems to be the first ever discovered evolutionary reconstruction [6], the mosaic of these hybrid between an RNA and a DNA virus (hence other key characteristics of viruses implies complex appropriately named RNA­DNA Hybrid Virus, or processes of multiple loss of ancestral genes (in particular, RDHV). In this particular case, the genome is in the DNA those for capsid proteins), gene exchange between distant form and the replication machinery derives from a DNA viruses and transfer of viruses between distant hosts virus whereas the capsid is of RNA viral origin. It remains (such as fungi, plants, animals and protists, but possibly to be seen what other surprising chimeras pop up when also between bacteria and fungi, even if only via endo­ diverse habitats are explored deeply and systematically. symbiosis) [9]. Beyond discovering strange chimeras, metagenomics Certainly, the phylogeny of the RdRps only reflects the has the potential to change the existing fundamental evolutionary history of this gene that is congruent with ideas on the evolution of RNA viruses. Almost all the histories of other genes only in some limited, tight extremely diverse RNA viruses infect various eukaryotes. groups of viruses, but by no account the evolutionary The only two known families of bacterial RNA viruses, history of viruses themselves. A comprehensive history Leviviridae and Cystoviridae, might not even have a should integrate the histories of individual genes and can common origin with the majority of eukaryotic RNA only adequately be conceptualized as a network of multiple viruses [6], the evolutionary relationship between evolutionary connections at the level of genes or even Leviviridae and Narnaviridae notwithstanding. So where parts of genes encoding distinct protein domains. Huiquan does the bulk of RNA viruses come from? A hypothesis Liu and colleagues have made an interesting new has been proposed that the RdRp was derived from the contribution to unfolding the network of evolutionary reverse transcriptase of a bacterial retro­transcribing relationships between diverse groups of dsRNA viruses element and the other genes from different bacteriophage that all have been shown to contain the S7 RNA­binding and bacterial sources [6]. However, metagenomics has domain within distinct multidomain proteins (Figure 1). recently offered a viable alternative: positive­strand RNA This finding implies that gene transfer between RNA viruses might have pre­existed in archaeal ancestors of viruses is even more pervasive than previously suspected eukaryotes. The first putative archaeal RNA virus has and further suggests that acquisition of the S7 domain is been isolated from near­boiling, archaea­dominated geo­ beneficial for the replication of diverse dsRNA viruses. thermal springs

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