Viruses take center stage in cellular evolution

Abstract

The origins of viruses are shrouded in mystery, but advances in genomics and the discovery of highly complex giant DNA viruses have stimulated new hypotheses that DNA viruses were involved in the emergence of the eukaryotic cell nucleus, and that they are worthy of being considered as living organisms.

Figure 1

A possible iterative scenario for viral eukaryogenesis and nuclear viriogenesis. (a) A primitive DNA virus (a bacteriophage ancestor) gets trapped within an RNA cell and becomes a primitive nucleus. (b) Cellular genes are progressively recruited to the enlarging nucleus because of the selective advantages of DNA biochemistry. (c) For a while this situation remains unstable and reversible, allowing new 'pre-eukaryotic viruses' to be created. These viruses reinfect other cells at various stages of this iterative process. (d) This hypothetical scheme provides a mechanism for the emergence of various overlapping but not monophyletic virus lineages as well as for the rapid reassortment of genes from the viral and cellular pools before they reach their 'Darwinian threshold' [29], that is, (e) the evolution of a stable eukaryotic cell with a fully DNA nuclear genome.

Figure 2

What is a virus? The life cycle of a complex dsDNA virus (for example NCLDVs) is shown. (a) A virus particle infects the cell and releases its DNA into the cytoplasm. (b) The viral DNA replicates and capsid proteins are synthesized within a 'virus factory' in the cytoplasm to which are recruited cellular ribosomes and the protein-synthesis machinery, as well as mitochondria to provide ATP. (c) New infectious viral particles are produced (while the nucleus is fading) and (d) released from the cell to begin another round of infection and replication. I propose that the true nature of complex eukaryotic dsDNA viruses is found in the transient virus factory they produce at each generation, rather than in the reproductive virus particle with which they have been equated. The virus factory is proposed to represent the result of the progressive reductive evolution of an obligate parasitic cellular organism, committed to the viral evolutionary pathway by the loss of a functional translation machinery. For a viral organism, the virus factory exhibits all the properties of the soma, in which genes are expressed, while the particle state corresponds to the germline (sensu August Weismann [28]) which remains unchanged. If we follow this line of thought, one might think of infection as being analogous with fertilization and the production of new virus particles as being akin to the formation of gametes.