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Informational Gene Phylogenies Do Not Support a Fourth Domain of Life for Nucleocytoplasmic Large DNA Viruses

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  • Tom A Williams
  • T Martin Embley
  • Eva Heinz

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.

Suggested Citation

  • Tom A Williams & T Martin Embley & Eva Heinz, 2011. "Informational Gene Phylogenies Do Not Support a Fourth Domain of Life for Nucleocytoplasmic Large DNA Viruses," PLOS ONE, Public Library of Science, vol. 6(6), pages 1-11, June.
  • Handle: RePEc:plo:pone00:0021080
    DOI: 10.1371/journal.pone.0021080
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    References listed on IDEAS

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    1. Maria C. Rivera & James A. Lake, 2004. "The ring of life provides evidence for a genome fusion origin of eukaryotes," Nature, Nature, vol. 431(7005), pages 152-155, September.
    2. Hervé Philippe & Henner Brinkmann & Richard R. Copley & Leonid L. Moroz & Hiroaki Nakano & Albert J. Poustka & Andreas Wallberg & Kevin J. Peterson & Maximilian J. Telford, 2011. "Acoelomorph flatworms are deuterostomes related to Xenoturbella," Nature, Nature, vol. 470(7333), pages 255-258, February.
    3. Ivan Hrdy & Robert P. Hirt & Pavel Dolezal & Lucie Bardonová & Peter G. Foster & Jan Tachezy & T. Martin Embley, 2004. "Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I," Nature, Nature, vol. 432(7017), pages 618-622, December.
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