Elsevier

Research in Microbiology

Volume 160, Issue 7, September 2009, Pages 466-472
Research in Microbiology

The origin of viruses

https://doi.org/10.1016/j.resmic.2009.07.008Get rights and content

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 the virosphere 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.

Introduction

It was recently proposed that 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 contains 33 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 universal optimized 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 of capsid 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.

Section snippets

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 to this traditional view, viruses are essentially “gene robbers” or “pickpockets” that evolve by recruiting cellular genes (for a recent opinion paper illustrating this view, see [57]). In that paradigm, all viral genes should have a cellular origin in fine. As a consequence, the very existence

Viruses, as cellular organisms producing virions

The idea that viruses, as defined above, originated after the first cells is in line with the recent suggestion that viruses should be considered as a particular type of living cellular organism [38], [36]. Lwoff noticed a long time ago that infection of bacteria by a “bacteriophage” transforms the infected cell into a viral factory [53]. In many cases, the genome of the infected cell is destroyed and the only genome remaining operational in the cellular body is the viral genome (for a recent

The impact of viruses on the evolution of Life

The time scale of viral evolution and the diversity of viral lineages that emerged during that time would explain why viral-specific genes now seem to outnumber cellular ones in metagenomic studies [12], [3], forming a huge reservoir of molecular biodiversity. The fact that viral genes have probably always outnumbered cellular ones implies that more genes have been transferred from viruses to cells than the opposite during the history of Life [38]. In complete contradiction with the view of

The origin of virions

Viruses originated from the association of a replicon, a capsid and the associated genome packaging, entry and extrusion mechanisms. The origin of replicons is a general problem, which encompasses both the origin of viruses and those of cells. The most specific aspect of the origin of viruses is therefore the problem of the origin of virions. Virions are usually formed by a nucleoprotein core which is surrounded by capsid proteins. Some virions contain a lipid membrane that can be located

How many viral lineages?

Structural analysis of modern virions (especially of capsid proteins) has revealed that capsids evolved independently at least twice [4], [5], [6], [48]. A first type of capsid is characterized by proteins with either single or double-jelly-roll folds [1], [5], [6], [48]. These structures are present in the capsid proteins of both RNA and DNA viruses and of viruses infecting the three domains of Life, indicating that capsids based on jelly-roll proteins already had been evolved before the LUCA,

The universal viral network of Life

It has been suggested that viral lineages which are based on virion structure should be considered true viral lineages, with the capsid being the hallmark of viruses [5]. This notion causes a problem, considering that different viruses with evolutionarily related virions can have non-homologous replication machineries and vice-versa [50], [46], [47]. Indeed, as previously discussed, viruses as organisms can be viewed as assemblages of several gene clusters or cassettes encoding “molecular

Conclusion: viruses testify of our ancient history

Finally, is it relevant to discuss the origin of viruses in the context of the origin of Life? Although viruses (defined as capsid-encoding organisms) clearly originated at a relatively late stage of the evolution of Life (the second age of the RNA world, after the “invention” of modern proteins [30]), they are an intrinsic part of Life as we know it and, accordingly, the origin of life encompasses the origin of viruses. Furthermore, from their very ancient origin, modern viruses still appear

Acknowledgments

We would like to thank Simonetta Gribaldo for stimulating and critical discussions on the nature of viruses.

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