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. 2006 Mar 7;103(10):3669-74.
doi: 10.1073/pnas.0510333103. Epub 2006 Feb 27.

Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain

Patrick Forterre  1
Affiliations

Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain

Patrick Forterre. Proc Natl Acad Sci U S A. .

Abstract

The division of the living world into three cellular domains, Archaea, Bacteria, and Eukarya, is now generally accepted. However, there is no consensus about the evolutionary relationships among these domains, because all of the proposed models have a number of more or less severe pitfalls. Another drawback of current models for the universal tree of life is the exclusion of viruses, otherwise a major component of the biosphere. Recently, it was suggested that the transition from RNA to DNA genomes occurred in the viral world, and that cellular DNA and its replication machineries originated via transfers from DNA viruses to RNA cells. Here, I explore the possibility that three such independent transfers were at the origin of Archaea, Bacteria, and Eukarya, respectively. The reduction of evolutionary rates following the transition from RNA to DNA genomes would have stabilized the three canonical versions of proteins involved in translation, whereas the existence of three different founder DNA viruses explains why each domain has its specific DNA replication apparatus. In that model, plasmids can be viewed as transitional forms between DNA viruses and cellular chromosomes, and the formation of different levels of cellular organization (prokaryote or eukaryote) could be traced back to the nature of the founder DNA viruses and RNA cells.

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Conflict of interest statement

Conflict of interest statement: No conflicts declared.

Figures

Fig. 1.
Fig. 1.
The three viruses, three domains theory. Dotted lines correspond to RNA cell lineages, and bold lines correspond to DNA cell lineages. FvA, FvB, and FvE are founder viruses for Archaea, Bacteria, and Eukarya, respectively. The cellular tree is rooted in the “bacterial branch” (1), but other rootings are possible (discussed in ref. 6). The arrows between FvA and FvE are connected to symbolize specific evolutionary relationships between the two viruses that provide their DNA replication machineries to the archaeal and the eukaryal domains.
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