Abstract
AbstractDuring the first half of the twentieth century, many scientists considered viruses the smallest living entities and primitive life forms somehow placed between the inert world and highly evolved cells. The development of molecular biology in the second half of the century showed that viruses are strict molecular parasites of cells, putting an end to previous virocentric debates that gave viruses a primeval role in the origin of life. Recent advances in comparative genomics and metagenomics have uncovered a vast viral diversity and have shown that viruses are active regulators of cell populations and that they can influence cell evolution by acting as vectors for gene transfer among cells. They have also fostered a revival of old virocentric ideas. These ideas are heterogeneous, extending from proposals that consider viruses functionally as living beings and/or as descendants of viral lineages that preceded cell evolution to other claims that consider viruses and/or some viral families a fourth domain of life. In this article, we revisit these virocentric ideas and analyze the place of viruses in biology in light of the long-standing dichotomic debate between metabolist and geneticist views which hold, respectively, that self-maintenance (metabolism) or self-replication and evolution are the primeval features of life. We argue that whereas the epistemological discussion about whether viruses are alive or not and whether some virus-like replicators precede the first cells is a matter of debate that can be understood within the metabolism-versus-genes dialectic; the claim that viruses form a fourth domain in the tree of life can be solidly refuted by proper molecular phylogenetic analyses and needs to be removed from this debate.
Highlights
Viruses were discovered at the end of the nineteenth century following several observations
Either we accept that anything that can evolve or be evolved is alive, which would include genes and memes in general; or we extend the definition of the term virus to include a hypothetical capacity for self-replication
Using better taxon sampling and adequate models of sequence evolution, it can be shown that the vast majority of homologues to cellular genes present in giant viruses correspond to transfers from the host to its virus; and that nucleo-cytoplasmic large DNA viruses (NCLDV) genes do not form a monophyletic group at the base of eukaryotes, but appear dispersed within the eukaryotic tree close to their respective hosts (López-García and Moreira 2009; Moreira 2000; Moreira and Brochier-Armanet 2008; Moreira and Lopez-Garcia 2005; Moreira and López-García 2009; Williams et al 2011)
Summary
Viruses were discovered at the end of the nineteenth century following several observations.
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