Analysis | Published:

The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups

Nature Reviews Microbiology volume 6, pages 925939 (2008) | Download Citation

Abstract

The recent discovery of RNA viruses in diverse unicellular eukaryotes and developments in evolutionary genomics have provided the means for addressing the origin of eukaryotic RNA viruses. The phylogenetic analyses of RNA polymerases and helicases presented in this Analysis article reveal close evolutionary relationships between RNA viruses infecting hosts from the Chromalveolate and Excavate supergroups and distinct families of picorna-like viruses of plants and animals. Thus, diversification of picorna-like viruses probably occurred in a 'Big Bang' concomitant with key events of eukaryogenesis. The origins of the conserved genes of picorna-like viruses are traced to likely ancestors including bacterial group II retroelements, the family of HtrA proteases and DNA bacteriophages.

Key points

  • RNA viruses, which are most common in eukaryotes, are among the simplest forms of life.

  • Genomic and metagenomic studies have highlighted remarkable diversity of a major class of RNA viruses, the extended picornavirus-like superfamily.

  • Phylogenetic analysis reveals close evolutionary relationships between RNA viruses infecting unicellular eukaryotes and distinct families of picorna-like viruses of plants and animals.

  • This suggests that diversification of picorna-like viruses antedated radiation of the eukaryotes and probably occurred in a 'Big Bang' concomitant with the key events of eukaryogenesis.

  • The origins of the conserved genes of picorna-like viruses can be traced to specific prokaryotic ancestors.

  • The Big Bang of picorna-like virus evolution might have been triggered by chance assembly of these ancestral genes at the earliest stages of eukaryogenesis.

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Acknowledgements

This paper is dedicated to Professor Vadim I. Agol. We thank V. Agol and T. Senkevich for critical reading of the manuscript and useful comments. E.V.K. and Y.I.W. are supported by the Department of Health and Human Services (National Library of Medicine, National Institutes for Health) intramural research funds. The research in V.V.D.'s laboratory is partially supported by National Institutes for Health grant GM053190 and BARD award no. IS-3,784-05.

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Affiliations

  1. National Center for Biotechnology Information, National Institutes of Health, Bethesda, Maryland 20894, USA.

    • Eugene V. Koonin
    •  & Yuri I. Wolf
  2. National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research Agency, 2-17-5 Maruishi, Hiroshima, 739-0452, Japan.

    • Keizo Nagasaki
  3. Department of Botany and Plant Pathology and Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon 97331, USA.

    • Valerian V. Dolja

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Correspondence to Eugene V. Koonin or Valerian V. Dolja.

Supplementary information

Glossary

Virosphere

Also termed virus world, the virosphere is the entirety of viruses and virus-like agents comprising a genetic pool that is continuous in space and time and encompasses, in particular, hallmark viral genes that encode essential functions of many diverse viruses but are not found in genomes of cellular life forms.

Superfamily

In this context, a superfamily is a large group of viral families that are thought to have evolved from a common ancestor.

Picornaviruses

Narrowly defined, picornaviruses are a family of small, positive-strand RNA viruses that infect animals including humans (for example, poliovirus and foot-and-mouth disease virus). Broadly defined, the superfamily of picorna-like viruses consists of many families of RNA viruses that infect animals, plants and diverse unicellular eukaryotes, and appear to be evolutionarily related to picornaviruses.

Jelly-roll fold

The jelly-roll fold is a characteristic structural fold of the capsid proteins that comprise the icosahedral capsids of a variety of viruses including most of the picorna-like viruses.

Maximum likelihood

Generally, maximum likelihood is the statistical methodology used to fit a mathematical model of a process to the available data. In the context of phylogenetic analysis, maximum-likelihood methods use evolution models of various degrees of complexity to infer probability distributions for all possible topologies of a phylogenetic tree and, accordingly, assign likelihood values to particular topologies.

Clade

A clade is a taxonomic group that consists of a single common ancestor and all its descendants; in a phylogenetic tree, a clade is always either a terminal branch or a compact subtree.

Horizontal virus transfer

(HVT). Cross-species virus transmission and adaptation to a new host.

Retroelements

Diverse genetic elements that encode a reverse transcriptase and, accordingly, replicate through a genetic cycle that includes a step of DNA synthesis on a RNA template.

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https://doi.org/10.1038/nrmicro2030

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