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The Evolutionary Loss of RNAi Key Determinants in Kinetoplastids as a Multiple Sporadic Phenomenon

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Abstract

We screened the genomes of a broad panel of kinetoplastid protists for genes encoding proteins associated with the RNA interference (RNAi) system using probes from the Argonaute (AGO1), Dicer1 (DCL1), and Dicer2 (DCL2) genes of Leishmania brasiliensis and Crithidia fasciculata. We identified homologs for all the three of these genes in the genomes of a subset of these organisms. However, several of these organisms lacked evidence for any of these genes, while others lacked only DCL2. The open reading frames encoding these putative proteins were structurally analyzed in silico. The alignments indicated that the genes are homologous with a high degree of confidence, and three-dimensional structural models strongly supported a functional relationship to previously characterized AGO1, DCL1, and DCL2 proteins. Phylogenetic analysis of these putative proteins showed that these genes, when present, evolved in parallel with other nuclear genes, arguing that the RNAi system genes share a common progenitor, likely across all Kinetoplastea. In addition, the genome segments bearing these genes are highly conserved and syntenic, even among those taxa in which they are absent. However, taxa in which these genes are apparently absent represent several widely divergent branches of kinetoplastids, arguing that these genes were independently lost at least six times in the evolutionary history of these organisms. The mechanisms responsible for the apparent coordinate loss of these RNAi system genes independently in several lineages of kinetoplastids, while being maintained in other related lineages, are currently unknown.

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Acknowledgements

This work has been funded by the Grant from the National Science Foundation’s Assembling the Tree of Life program (G.A. Buck, Award #080056); the grant from the NIH (S.M. Beverley, award #RO1AI029646), and grants from the Brazilian agencies CNPq and CAPES to MMGT. JMPA is supported by FAPESP, Brazil (Grant #2013/14622-3, São Paulo Research Foundation). AGCM has PhD fellowship from CNPq (PROTAX). The authors are grateful to Marta Campaner for cultures of parasites, Flávia Maia da Silva and Luciana Lima for the preparation of DNAs used for genome sequencing, and the personnel of the Nucleic Acids Research Facilities (NARF) at VCU.

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Authors and Affiliations

  1. Department of Microbiology and Immunology and the Center for the Study of Biological Complexity, Virginia Commonwealth University, Richmond, VA, USA

    Andrey V. Matveyev, João M. P. Alves, Myrna G. Serrano, Vladimir Lee, Ana M. Lara & Gregory A. Buck

  2. Department of Biochemistry and Molecular Biology, Virginia Commonwealth University, Richmond, VA, USA

    William A. Barton

  3. Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, MO, USA

    Stephen M. Beverley

  4. Department of ParasitologyICB, University of São Paulo, São Paulo, Brazil

    João M. P. Alves, André G. Costa-Martins, Erney P. Camargo & Marta M. G. Teixeira

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  1. Andrey V. Matveyev
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  3. Myrna G. Serrano
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  4. Vladimir Lee
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Correspondence to Andrey V. Matveyev.

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Matveyev, A.V., Alves, J.M.P., Serrano, M.G. et al. The Evolutionary Loss of RNAi Key Determinants in Kinetoplastids as a Multiple Sporadic Phenomenon. J Mol Evol 84, 104–115 (2017). https://doi.org/10.1007/s00239-017-9780-1

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