Virus

Virus Research 117 (2006) 5–16

Review

The origin of viruses and their possible roles in major
evolutionary transitions
Patrick Forterre a,b,∗
a

Institut de G´ n´ tique et Microbiologie, CNRS UMR 8621, Universit´ Paris-Sud, 91405 Orsay Cedex, France
ee
e
b Institut Pasteur, 25 rue du Docteur Roux, 75015 Paris, France
Available online 14 February 2006

Abstract
Viruses infectingcells from the three domains of life, Archaea, Bacteria and Eukarya, share homologous features, suggesting that viruses
originated very early in the evolution of life. The three current hypotheses for virus origin, e.g. the virus first, the escape and the reduction
hypotheses are revisited in this new framework. Theoretical considerations suggest that RNA viruses may have originated in thenucleoprotein
world by escape or reduction from RNA-cells, whereas DNA viruses (at least some of them) might have evolved directly from RNA viruses. The
antiquity of viruses can explain why most viral proteins have no cellular homologues or only distantly related ones. Viral proteins have replaced
the ancestral bacterial RNA/DNA polymerases and primase during mitochondrial evolution. It has beensuggested that replacement of cellular
proteins by viral ones also occurred in early evolution of the DNA replication apparatus and/or that some DNA replication proteins originated
directly in the virosphere and were later on transferred to cellular organisms. According to these new hypotheses, viruses played a critical role in
major evolutionary transitions, such as the invention of DNA and DNAreplication mechanisms, the formation of the three domains of life, or else,
the origin of the eukaryotic nucleus.
© 2006 Elsevier B.V. All rights reserved.
Keywords: Virus origin; RNA world; RNA/DNA transition; Mimivirus; DNA origin; DNA replication; Nucleus origin; LUCA; Universal tree of life

Contents
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3.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Viruses as old players in life evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The three hypothesesfor virus origin revisited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1. The virus-first hypothesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .3.2. The escape hypothesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.3. The reduction hypothesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . .
4. The origin of DNA viruses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5. Viruses and the puzzling phylogenomic distribution of DNA replication proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . .
6. Viruses and the origin of DNA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7. Viruses and the origin of the three modern cellular domains . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ....