The protist Trichomonas vaginalis harbors multiple lineages of transcriptionally active Mutator-like elements

Fabrício R Lopes,Marlene Benchimol,Gustavo GL Costa,Gonçalo AG Pereira,Claudia MA Carareto,Joana C Silva

doi:10.1186/1471-2164-10-330

Abstract

BackgroundFor three decades the Mutator system was thought to be exclusive of plants, until the first homolog representatives were characterized in fungi and in early-diverging amoebas earlier in this decade.ResultsHere, we describe and characterize four families of Mutator-like elements in a new eukaryotic group, the Parabasalids. These Trichomonas vaginalis Mutator- like elements, or TvMULEs, are active in T. vaginalis and patchily distributed among 12 trichomonad species and isolates. Despite their relatively distinctive amino acid composition, the inclusion of the repeats TvMULE1, TvMULE2, TvMULE3 and TvMULE4 into the Mutator superfamily is justified by sequence, structural and phylogenetic analyses. In addition, we identified three new TvMULE-related sequences in the genome sequence of Candida albicans. While TvMULE1 is a member of the MuDR clade, predominantly from plants, the other three TvMULEs, together with the C. albicans elements, represent a new and quite distinct Mutator lineage, which we named TvCaMULEs. The finding of TvMULE1 sequence inserted into other putative repeat suggests the occurrence a novel TE family not yet described.ConclusionThese findings expand the taxonomic distribution and the range of functional motif of MULEs among eukaryotes. The characterization of the dynamics of TvMULEs and other transposons in this organism is of particular interest because it is atypical for an asexual species to have such an extreme level of TE activity; this genetic landscape makes an interesting case study for causes and consequences of such activity. Finally, the extreme repetitiveness of the T. vaginalis genome and the remarkable degree of sequence identity within its repeat families highlights this species as an ideal system to characterize new transposable elements.

Highlights

For three decades the Mutator system was thought to be exclusive of plants, until the first homolog representatives were characterized in fungi and in early-diverging amoebas earlier in this decade
While TvMULE1 is a member of the MuDR clade predominantly from plants, the other three Trichomonas vaginalis Mutatorlike elements (TvMULEs) represent a new and quite distinct Mutator lineage, expanding the taxonomic distribution and the range of functional motif of Mutator-like elements (MULEs) among eukaryotes
The manual inspection of a combination of sequence similarity searches and consensus sequence building techniques and the presence of putative, imperfect, terminal inverted repeats (TIRs) resulted in the definition four new Mutator-like transposable element families represented by the consensus sequence of which we termed TvMULE1, TvMULE3 and TvMULE4 (Figure 1) and TvMULE2 represented by the

Summary

Introduction

For three decades the Mutator system was thought to be exclusive of plants, until the first homolog representatives were characterized in fungi and in early-diverging amoebas earlier in this decade. TEs can lead to genome expansion and contraction [7,8,9], transduction and amplification of host gene fragments [10,11] and increase the variability of protein repertories [12,13,14,15,16,17,18,19,20] Given this enormous potential as a source of genetic novelty, considerable effort has been devoted by the scientific community to the characterization of new TEs in the plethora of new genomes and transcriptomes available in public databases, in organisms for which the knowledge about TEs is scarce. While some families of TEs are found across most taxa surveyed, others appear to have a restricted host distribution; the Mutator system in plants was an example of the latter This notion was recently dispelled by the identification and extensive characterization of Mutator homologs in the first non-plant species [21,22,23,24]. Consensus sequences of new representatives of this TE family obtained from a broad range of species have been reported in Repbase Reports within the past few years: CEMUDR1-2 from Caenoharbidtis elegans [25,26]; MuDR12_TP in the diatom Thalassiosira pseudonana [27,28]; MuDr1-2_NV in the starlet sea anemone Nematostella vectensis [29,30]; MuDR1x-2x_SM in the planarian Schmidtea mediterranea [31,32] and MuDr1x-2x_AP in the insect Acyrthosiphon pisum [33,34]

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Conclusion