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Phylogenetic Analysis of the Complete Genome Sequence of Encephalitozoon cuniculi Supports the Fungal Origin of Microsporidia and Reveals a High Frequency of Fast-Evolving Genes

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Abstract

Microsporidia are unicellular eukaryotes living as obligate intracellular parasites. Lacking mitochondria, they were initially considered as having diverged before the endosymbiosis at the origin of mitochondria. That microsporidia were primitively amitochondriate was first questioned by the discovery of microsporidial sequences homologous to genes encoding mitochondrial proteins and then refuted by the identification of remnants of mitochondria in their cytoplasm. Various molecular phylogenies also cast doubt on the early divergence of microsporidia, these organisms forming a monophyletic group with or within the fungi. The 2001 proteins putatively encoded by the complete genome of Encephalitozoon cuniculi provided powerful data to test this hypothesis. Phylogenetic analysis of 99 proteins selected as adequate phylogenetic markers indicated that the E. cuniculi sequences having the lowest evolutionary rates preferentially clustered with fungal sequences or, more rarely, with both animal and fungal sequences. Because sequences with low evolutionary rates are less sensitive to the long-branch attraction artifact, we concluded that microsporidia are evolutionarily related to fungi. This analysis also allowed comparing the accuracy of several phylogenetic algorithms for a fast-evolving lineage with real rather than simulated sequences.

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Authors and Affiliations

  1. Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Claude Bernard Lyon I, 43 boulevard du 11 Novembre 1918, Villeurbanne, 69622, France

    Fabienne Thomarat & Manolo Gouy

  2. Laboratoire de Biologie des Protistes, UMR CNRS 6023, Université Blaise Pascal, Aubière Cedex, 63117, France

    Christian P. Vivarès

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  1. Fabienne Thomarat
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  2. Christian P. Vivarès
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  3. Manolo Gouy
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Correspondence to Manolo Gouy.

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Reviewing Editor: Dr. Wen-Hsiung Li

Supplementary material is available at http://pbil.univ-lyon1.fr/datasets/Thomarat2003/

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Thomarat, F., Vivarès, C.P. & Gouy, M. Phylogenetic Analysis of the Complete Genome Sequence of Encephalitozoon cuniculi Supports the Fungal Origin of Microsporidia and Reveals a High Frequency of Fast-Evolving Genes. J Mol Evol 59, 780–791 (2004). https://doi.org/10.1007/s00239-004-2673-0

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