Abstract
Mimivirus is a nucleocytoplasmic large DNA virus (NCLDV) with a genome size (1.2 Mb) and coding capacity ( 1000 genes) comparable to that of some cellular organisms. Unlike other viruses, Mimivirus and its NCLDV relatives encode homologs of broadly conserved informational genes found in Bacteria, Archaea, and Eukaryotes, raising the possibility that they could be placed on the tree of life. A recent phylogenetic analysis of these genes showed the NCLDVs emerging as a monophyletic group branching between Eukaryotes and Archaea. These trees were interpreted as evidence for an independent “fourth domain” of life that may have contributed DNA processing genes to the ancestral eukaryote. However, the analysis of ancient evolutionary events is challenging, and tree reconstruction is susceptible to bias resulting from non-phylogenetic signals in the data. These include compositional heterogeneity and homoplasy, which can lead to the spurious grouping of compositionally-similar or fast-evolving sequences. Here, we show that these informational gene alignments contain both significant compositional heterogeneity and homoplasy, which were not adequately modelled in the original analysis. When we use more realistic evolutionary models that better fit the data, the resulting trees are unable to reject a simple null hypothesis in which these informational genes, like many other NCLDV genes, were acquired by horizontal transfer from eukaryotic hosts. Our results suggest that a fourth domain is not required to explain the available sequence data.
Highlights
Resolving the tree of life is among the most interesting and challenging questions in evolutionary biology
The small genomes of viruses did not contain enough information to reliably position them on the tree of life [4]. The latter argument was weakened by the discovery of Mimivirus, a nucleocytoplasmic large DNA virus (NCLDV) with a genome of unprecedented size (1.2Mb) and coding capacity (w 1,000 ORFs), exceeding that of many cellular organisms [5,6]
A subsequent re-analysis of the dataset used in [6] indicated that the position of Mimivirus was an artifact: the genes that were concatenated to build the phylogeny had been acquired by horizontal transfer (HGT) from different sources, resulting in an inconsistent phylogenetic signal that placed them as the outgroup to Eukaryotes [8]
Summary
Resolving the tree of life is among the most interesting and challenging questions in evolutionary biology. Modelling compositional heterogeneity For each of the alignments, one analysis was performed under the JTT, the WAG and the LG rate exchange matrix using one compositional vector, estimated from the data during the run.
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