Viruses in Biology

Abstract

During 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.

Evolution of viruses and cells: do we need a fourth domain of life to explain the origin of eukaryotes?

“…mitochondrial RNA polymerase [39] and DNA primase [40]), but, in general, they concern the replacement of activities already present in cells by their viral counterparts rather than the import of truly new functions. Thus, the claimed viral role as the creators of major cellular traits has most likely been overestimated as a consequence of improper (or simply absent) phylogenetic analysis [33,87]. Essential eukaryotic structures such as the nucleus and the nuclear pore or the complex endomembrane system of eukaryotic cells remain fundamentally unexplained by any viral-based model for the origin of eukaryotes.…”

“…The discovery of giant viruses and their enigmatic phylogenetic position attracted much scientific attention and, incidentally, served to revive more or less old ideas about the role of viruses in early evolution [32,33]. In parallel with the immense recent improvement of the scientific knowledge on the diversity of viruses infecting members of the three domains of life, speculations on viruses depicted as creative evolutionary agents at the origin of essential traits of cellular organisms have flourished.…”

Towards an Evolutionary Perspective in Teaching and Popularizing Microbiology

“…Specifically, in the case of viruses, it is important to discuss their existence beyond the negative perspective that is usually presented. One way to achieve this is to explore hypotheses about the role of viruses in the origin of life and the evolution of the first cells ( 28 ), as well as discussing the ability of viruses to introduce new information into the host genome, emphasizing their co-evolution and their major influence in the evolutionary history of several living beings ( 29 , 30 ). Another approach to changing the common view of viruses is to introduce new topics, such as the occurrence of giant viruses in nature ( 31 ).…”

Understanding viruses: Philosophical investigations

“…has been raised repeatedly throughout the history of Scola et al, 2008), had the potential to radically modify our views about the living or nonliving status of viruses (mainly because it has become very difficult to draw a boundary between some cellular organisms strongly dependent on their host and harbouring less than a minimal genome and the giant viruses that encode many genes and exhibit some degree of autonomy (Claverie & Abergel, 2010; this special issue)) and/or the role viruses could have played in the origins of life (Forterre, 2010b;Raoult & Forterre, 2008). These views have been met with scepticism by many other virologists (López-García, 2012; López-García & Moreira, 2012;Moreira & López-García, 2009), giving rise to a strong controversy (see, e.g., (Villarreal, 2004), (Villarreal & Witzany, 2010); see also Claverie and Abergel, Forterre, as well as van Regenmortel, this special issue).…”