3. The three hypotheses for virus origin revisited
\nThe hypothesis that viruses were already present before the emergence of modern DNA-cells opens
\nnew perspectives about their origin and suggests we revisit the three classical hypotheses in this new
\ncontext.
\n3.1. The virus-first hypothesis
\nThe virus-first hypothesis has been revived in the last decade by Wolfram Zillig who suggested that
\nviruses originated in the prebiotic word, using the primitive soup as a host (Prangishvili et al., 2001).
\nSuch hypothesis is in line with the view, advocated by several molecular biologists, that the formation of
\ncells occurred relatively late in the evolution of life. It was common for some time to imagine the RNA
\nworld as a community of free molecules competing with each others (Gilbert, 1986). Recently, some
\nauthors have even proposed that the Last Universal Common Ancestor (LUCA) was not a cellular entity
\n(Kandler, 1998; Martin and Russell, 2003; Koga et al., 1998). In particular, they suggested that cellular
\nmembranes originated independently after the divergence of Archaea and Bacteria, in order to explain
\nwhy archaeal lipids are so different from eukaryotic\/bacterial ones (with opposite stereochemistry and
\ndifferent carbon chains). If all life evolution from the very beginning up to LUCA occurred in an acellular
\ncontext, it is indeed possible to imagine that viruses first emerged as individual entities in a world of
\ncompeting proteins and nucleic acids, either bathing in a !primitive soup\u201d or located on a mineral
\nplatform. However, the hypothesis of a LUCA without membrane is contradicted by the existence of
\nhomologous proteins functioning at the membrane level that are encoded by all sequenced genomes
\nfrom the three domains of life, strongly suggesting that these proteins (hence a membrane) were
\nalready present in LUCA (Pereto et al., 2004). In fact, the first cells probably arose well before the
\nemergence of LUCA. For instance, it appears unlikely that a world of free molecules could have
\nevolved to such an extent to produce a ribozyme capable of synthesizing proteins (the ancestor of
\npresent-day ribosomes). Even in the early RNA world, a primitive metabolism should have produced at
\nleast precursors for RNA and lipid syntheses, as well as the energy required to perform these reactions.
\nIt is difficult to imagine the emergence of such a metabolism without Darwinian selection, and this
\nrequires the competition between well-defined individual entities (at least proto-cells). Since modern
\nviruses contain proteins, they should have originated after the emergence of the ancestral ribosome,
\ni.e. well after the apparition of primitive RNA-cells (in the second age of the RNA world, sensu Forterre,
\n2005). Accordingly, in my opinion, the virus first theory can be rejected for present-day viruses (even
\nviroids would need a suitable cellular environment providing nucleotides for their emergence). In this
\ncase, one is presently left with only two possibilities: either the first RNA viruses originated from RNA
\ncells by regressive evolution (a new version of the reduction theory), or from RNA fragments that
\nescaped from RNA cells (a new version of the escape theory).
\n3.2. The escape hypothesis
\nThe traditional hypothesis viewing viruses as elements of cell genomes that escaped from their cellular
\nenvironment, becoming autonomous and infectious selfish elements, is easier to defend in the context
\nof a pre-LUCA scenario for virus origin. In this context, one does not expect anymore any specific
\nrelationship between proteins encoded by viruses and those encoded by their hosts, since viruses now
\nderive from genome fragments escaped from cells predating LUCA. Furthermore, one can reasonably
\nassume that it was easier for a genome fragment to become autonomous in ancient RNA cells, since
\nthe different molecular mechanisms operating in these proto-cells were probably much simpler and less
\nintegrated than in modern DNA cells (Woese, 2002). In particular, it has been often argued that the
\ngenomes of ancestral RNA cells were fragmented (as in the case of modern double-stranded RNA
\nviruses). These genomes could have been composed of semi-autonomous chromosomes (possibly
\nformed by a few RNA genes) that were replicated independently and transferred randomly from cells to
\ncells (Woese, 1987 ; Poole et al., 1998). Some RNA chromosomes could have encoded a coat protein
\nthat helps the proto-virus to be transferred, finally becoming infectious (Fig. 2). This process would be
\nreminiscent of the moron theory proposed by Hendrix and co-workers for the origin of virus (Hendrix et
\nal., 2000). Although this theory was inferred from the observation that modern DNA viruses can easily
\nacquire more DNA by illegitimate recombination it can be easily extrapolated for the origin of RNA
\nviruses in the RNA world.
\n3.3. The reduction hypothesis
\nThe transformation of a cellular organism into a viral one could have been also much easier in a world
\nof RNA cells, again because these cells were much simpler than modern ones. Just as modern
\nparasites can loose part of their metabolic channels, an RNA-cell living as a parasitic endosymbiont in
\nanother RNA cell could have lost its own machinery for protein synthesis and for energy production,
\nusing instead those of the host (Fig. 2) (Forterre, 2005). In this model, viral capsids could have
\noriginated from the envelopes of RNA cells composed of identical proteins, resembling the S-layer of
\nmodern prokaryotes. The reduction hypothesis might have been driven by the harsh competition that
\nmost likely occurred between RNA cells all along the evolution of the RNA world. As a consequence of
\nthis competition, early life evolution probably went through several bottlenecks each time a crucial new
\nmolecular mechanism was invented. At each of these bottlenecks, the descendents of the individual
\nendorsed with such a great selective advantage (the winners) would have eliminated all other lineages
\nof proto-cells that previously coexisted with them (the losers). The only chance of survival for the losers
\nwas to become parasites of the winners. In this hypothesis, viruses evolved by parasitic reduction from
\nancient lineages of RNA cells that were out-competed in the Darwinian selection process, and thus
\ncould only survive by parasiting the winner of this competition (Forterre, 1992).
\nFig. 2. Two alternative hypotheses for the origin of viruses in the second age of the RNA world (after invention of protein
\nsynthesis), black circles correspond to translation machinery (e.g. ancestral ribosomes) and lines to linear RNA chromosomes.
\nUpper panel, the escape hypothesis: unequal cell division produces minicells with single chromosome (a or b) but no
\ntranslation apparatus. The chromosome a will be eliminated but chromosome b will survive because it is associated with a
\nproteins coat that allows its transfer into a new RNA cell, it becomes a virus. Lower panel, the reduction hypothesis: a small
\nRNA cell became an endosymbiont of a larger RNA cell. It looses its translation apparatus but continue to replicate
\nautonomously and become infectious (similar to some pathogenic bacteria in eukaryotic cells).<\/p>\n
————–<\/p>\n
3. A re-examination of the three virus origin hypotheses
\nThe possibility that viruses existed prior to the emergence of modern DNA-cells is raised.<\/p>\n
new perspectives on their origins and proposes revisiting the three classic hypotheses in this new study<\/p>\n
context.<\/p>\n
The virus-first hypothesis (3.1)<\/p>\n
Wolfram Zillig revived the virus-first hypothesis in the last decade, claiming that<\/p>\n
Viruses first appeared in the prebiotic world, using primitive soup as a host (Prangishvili et al., 2001).<\/p>\n
This hypothesis is consistent with the view held by several molecular biologists that the formation of<\/p>\n
Cells appeared relatively late in life’s evolution. For a long time, it was common to imagine the RNA.<\/p>\n
The world is viewed as a community of free molecules competing with one another (Gilbert, 1986).<\/p>\n","protected":false},"excerpt":{"rendered":"
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