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Research in Microbiology 160 (2009) 466e472

The origin of viruses
Patrick Forterre a,b,*, David Prangishvili b
b a Institut de Genetique et Microbiologie, Universite Paris-Sud, CNRS UMR 8621, 91405 Orsay Cedex, France ´ ´ ´ Biologie Moleculaire du Gene chez les Extremophiles, Departement de Microbiologie, Institut Pasteur, 75724 Paris Cedex 15, France ´ ` ˆ ´Received 9 June 2009; accepted 15 July 2009 Available online 30 July 2009

Abstract Viruses are parasitic organisms that live in infected cells and produce virions to disseminate their genes. Most viral proteins have no homologues in modern cells, in contradiction with the traditional view of viruses as pickpockets of cellular genes. This suggests that viral genes essentially originated in thevirosphere during replication of viral genomes and/or were recruited from cellular lineages now extinct. Some specific viral proteins are present in viruses infecting members of the three domains of Life, suggesting that viruses are indeed very ancient. In particular, structural analyses of capsid proteins have revealed that at least two types of virions originated independently before the LUCA(the Last Universal Cellular Ancestor). Although several hypotheses have been recently proposed to explain the origin of viruses, the emergence of virions, as a specific mechanism for gene dissemination, remains unexplained. Ó 2009 Elsevier Masson SAS. All rights reserved.
Keywords: Virus; Evolution; Last universal cellular ancestor; Origin of viral genes

1. Introduction It was recently proposedthat the living world can be divided between ribosome-encoding organisms (modern cells) and capsid-encoding organisms (viruses) [61]. The origin of modern cells is straightforward, i.e. they all descend from a single ancestor, the LUCA (the last universal cellular ancestor, or the Last Universal CenAncestor) [28,39]. The LUCA was already a complex organism, since the universal protein set contains33 ribosomal proteins [52]. This means that, in addition to the three rRNA molecules, the ribosome of the LUCA already contained AT LEAST these 33 proteins (it may have contained up to 67 proteins if ribosomal proteins specifically shared by Archaea and Eukarya were already present in the LUCA) [27]. In agreement with the assumption that the LUCA was a sophisticated organism, the modern universaloptimized genetic code [72] was probably already

operational in the LUCA. As all modern cells descend from the LUCA, it is theoretically possible (even if practically difficult) to draw a universal tree of Life connecting together all ribosome-encoding organisms [76,77,15]. In contrast, there is not a single informational molecule common to all viruses. In particular, structural analyses ofcapsid proteins indicate that different types of virions have been selected several times independently as modes of viral genes dissemination ([6] see below). Furthermore, new viruses have emerged during evolution by the mixing of different capsids and viral genomes [47,37]. Accordingly, it will never be possible to draw a universal tree of viruses analogous to the tree of the LUCA [37,57].Understanding how modern viruses originated thus appears to be a more complex problem from the start than understanding the evolutionary history of modern cells. 2. The nature and origin of viral genes For some time it has been assumed that viral genomes have been derived from genomes of modern cells (bacteriophages from bacterial genomes and eukaryotic viruses from eukaryotic chromosomes). According tothis traditional view, viruses

´ ´ ´ * Corresponding author. Institut de Genetique et Microbiologie, Universite Paris-Sud, CNRS UMR 8621, 91405 Orsay Cedex, France. Tel.: þ33 1 45 68 87 91; fax: þ33 1 45 68 88 84. E-mail address: (P. Forterre). 0923-2508/$ - see front matter Ó 2009 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.resmic.2009.07.008

P. Forterre, D....
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