ReviewThe origin of viruses and their possible roles in major evolutionary transitions
Introduction
The origin of viruses is still enigmatic and their nature controversial (in part for historical reasons, the existence of viruses challenging the cellular theory of life). It has been often stated that viruses are polyphyletic, i.e. that different viral lineages originated independently. In particular, RNA and DNA viruses were thought to be evolutionary unrelated. However, the overall similarity between virus structures – a protein coat enclosing a nucleoprotein filament – at least suggests a common mechanism for their appearance. Three hypotheses have been proposed to explain the emergence of viruses: (i) they are relics of pre-cellular life forms; (ii) they are derived by reduction from unicellular organisms (via parasitic-driven evolution); (iii) they originated from fragments of genetic material that escaped from the control of the cell and became parasitic (Luria and Darnell, 1967, Bandea, 1983, Forterre, 2003, Hendrix et al., 2000 and references herein).
The first hypothesis (here called the virus-first hypothesis) has been dismissed for a long time, since all present viruses are obligatory parasites requiring an intracellular development stage for their reproduction. The second hypothesis (here called the reduction hypothesis) was also usually rejected based on two arguments: (i) we don’t know any intermediate form between cells and viruses; and (ii) parasites derived from cells in the three domains of life, such as Mycoplasma in Bacteria, Microsporidia in Eukaryotes or Nanoarchaea in Archaea, have retained their cellular characters (i.e. their own ribosomes and complete machineries for protein synthesis and ATP production). The third hypothesis (here called the escape theory) became popular partly by default and partly because it was a priori supported by the observation that present-day viruses can integrate cellular genes into their own genomes. In this view, plasmids and mobile elements are often considered to be viral precursors. However, the escape hypothesis has also serious drawbacks since it does not specify how a free nucleic acid could have recruited a capsid and the complex mechanisms required by viruses to deliver their nucleic acid to their host cells. Furthermore, in its traditional version, the escape hypothesis predicts that bacteriophages originated from bacterial genomes and eukaryotic viruses from eukaryotic genomes. In this case, one expects to find evolutionary affinities between viral proteins encoded by viruses from one domain and their cellular homologues in that domain. However, this is often not the case; for instance, some proteins encoded by T4 bacteriophage are more related to proteins from eukaryotes or eukaryotic viruses than to their bacterial homologues (Miller et al., 2003, Gadelle et al., 2003). Furthermore, although more than 250 cellular genomes from the three domains have now been completely sequenced, most of the viral proteins detected in viral genomes have no cellular homologues (up to 90–100% in the genomes of archaeal viruses) (Prangishvili and Garrett, 2004).
At this point, one should realize that some of the major critics against the three above hypotheses have been made in the context of the present-day biosphere (i.e. modern viruses indeed need modern cells to replicate, modern cells cannot regress to viral forms, free DNA cannot recruit proteins from modern cells to form capsids, and so on). However, things may be different if viruses originated before the formation of modern cells (sensu Woese, 2002): Archaea, Bacteria and Eukarya. In this case, we are less constraint by the present reality to propose new evolutionary scenarii for the origin of viruses. Of course, such speculations should be made with caution, but one cannot expect to understand the origin of modern cells and viruses by sticking to the present context. In this review, I will discuss briefly how the three hypotheses for virus origin can be revisited if one considers that viruses originated before the Last Universal Cellular Ancestor (LUCA) from which the three cellular domains diverged. I will also present recent data and new hypotheses on the involvement of viruses in the origin and early evolution of modern DNA cells.
Section snippets
Viruses as old players in life evolution
The idea that viruses are ancient was first more easily accepted for RNA viruses, in relation with the RNA world theory. Several authors have convincingly argued that present RNA viruses could be relics of the RNA world, whereas Retroviruses and/or Hepadnaviruses could be relics of the RNA/DNA transition (Wintersberger and Wintersberger, 1987, Weiner and Maizels, 1993, Weiner and Maizels, 1994, Makeyev and Grimes, 2004). Such vision was boosted by the discovery of tRNA-like structure linked to
The three hypotheses for virus origin revisited
The hypothesis that viruses were already present before the emergence of modern DNA-cells open new perspectives about their origin, and suggests to revisit the three classical hypotheses in this new context.
The origin of DNA viruses
DNA viruses could have emerged either from RNA viruses or independently. It is often stated that both types of viruses indeed originated independently in agreement with the current idea that viruses are polyphyletic. However, in my opinion, the homologies that can be detected at the structural and mechanistic levels between viral RNA replicases/transcriptases, reverse transcriptases and some DNA polymerases (Hansen et al., 1997), or else between viral RNA and DNA helicases (Gorbalenya et al.,
Viruses and the puzzling phylogenomic distribution of DNA replication proteins
A major surprise that came out early from large-scale comparative genomics was the existence of two sets of non-homologous proteins for DNA replication, one in Bacteria, and the other common to Archaea and Eukarya (Leipe et al., 1999). These sets include the central components of bacterial replication forks: replicative DNA polymerase, DNA primase and replicative helicase. This puzzling situation was in fact already predicted in 1977 by Woese and Fox, based on their progenote theory (Woese and
Viruses and the origin of DNA
It is usually considered that RNA was “logically” replaced by DNA in the course of evolution for two reasons: (i) it is more stable, thanks to the removal of the reactive oxygen in position 2′ of the ribose; and (ii) modification in the genetic message produced by deamination of cytosine into uracil (a common spontaneous chemical reaction) can be recognized and repaired in DNA, but not in RNA. As a consequence of this stability and more faithful replication, the substitution of RNA by DNA as
Viruses and the origin of the three modern cellular domains
As mentioned previously, the hypothesis that DNA was transferred from viruses to cells, together with a complete machinery for its replication, was originally proposed to explain the existence of two sets of non-homologous DNA replication proteins, one in Bacteria, the other in Archaea and Eukarya. It was thus necessary to imagine at least two independent transfers to take into account this observation (Fig. 4A, B). Recently, I have suggested that three independent transfers of DNA from viruses
Viruses and the origin of the eukaryotic nucleus
Recent theories suggesting a viral origin for the eukaryotic nucleus are another example of the comeback made by viruses in the mind of evolutionists during the last five years. The origin of the eukaryotic nucleus is one of the great mysteries of early life evolution (Pennisi, 2004). It has been advocated by several authors that the nucleus originated from an ancient archaeon that was engulfed by a bacterial-like cell. However, this hypothesis does not explain the existence of many eukaryotic
The role of viruses in the evolution of mitochondria and chloroplasts
It is obvious now for everybody that viruses have played an important role in recent cellular evolution by transferring some of their genes to cellular organisms. However, it is usually considered that modifications introduced in cellular lineages by viruses are restricted to “superficial” traits which have a direct selective advantage for the cell in a specific environment (e.g. pathogenecity islands) but do not drastically change its genomic make-up. It is thus difficult for many biologists
Conclusion
For a long time, viruses were not included in the universal tree of life, since they had no ribosomal RNA. As seen in this review, if the viruses are brought back into the tree (in fact if the tree and its root are immersed in a viral ocean, as suggested by Bamford (2003)), one can propose radically new hypotheses to solve problems encountered in deciphering ancient relationships between the three domains and the history of DNA replication mechanisms.
A reappraisal of the role of viruses in
Acknowledgment
I would like to thank Eugene Koonin for inviting me to write this review.
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