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. 2009 Apr 28:9:86.
doi: 10.1186/1471-2148-9-86.

DIRS1-like retrotransposons are widely distributed among Decapoda and are particularly present in hydrothermal vent organisms

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DIRS1-like retrotransposons are widely distributed among Decapoda and are particularly present in hydrothermal vent organisms

Mathieu Piednoël et al. BMC Evol Biol. .

Abstract

Background: Transposable elements are major constituents of eukaryote genomes and have a great impact on genome structure and stability. Considering their mutational abilities, TEs can contribute to the genetic diversity and evolution of organisms. Knowledge of their distribution among several genomes is an essential condition to study their dynamics and to better understand their role in species evolution. DIRS1-like retrotransposons are a particular group of retrotransposons according to their mode of transposition that implies a tyrosine recombinase. To date, they have been described in a restricted number of species in comparison with the LTR retrotransposons. In this paper, we determine the distribution of DIRS1-like elements among 25 decapod species, 10 of them living in hydrothermal vents that correspond to particularly unstable environments.

Results: Using PCR approaches, we have identified 15 new DIRS1-like families in 15 diverse decapod species (shrimps, lobsters, crabs and galatheid crabs). Hydrothermal organisms show a particularly great diversity of DIRS1-like elements with 5 families characterized among Alvinocarididae shrimps and 3 in the galatheid crab Munidopsis recta. Phylogenic analyses show that these elements are divergent toward the DIRS1-like families previously described in other crustaceans and arthropods and form a new clade called AlDIRS1. At larger scale, the distribution of DIRS1-like retrotransposons appears more or less patchy depending on the taxa considered. Indeed, a scattered distribution can be observed in the infraorder Brachyura whereas all the species tested in infraorders Caridea and Astacidea harbor some DIRS1-like elements.

Conclusion: Our results lead to nearly double both the number of DIRS1-like elements described to date, and the number of species known to harbor these ones. In this study, we provide the first degenerate primers designed to look specifically for DIRS1-like retrotransposons. They allowed for revealing for the first time a widespread distribution of these elements among a large phylum, here the order Decapoda. They also suggest some peculiar features of these retrotransposons in hydrothermal organisms where a great diversity of elements is already observed. Finally, this paper constitutes the first essential step which allows for considering further studies based on the dynamics of the DIRS1-like retrotransposons among several genomes.

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Figures

Figure 1
Figure 1
Complete structure of DIRS1-like retrotransposons indicating the position of degenerate primers along the pol region. A. Structure of the DIRS1 element identified in the slime mold Dictyostelium discoideum. The inverted terminal repeats (ITR) and the Internal Complementary Region (ICR) are represented by black triangles and hatched box, respectively. The three ORFs, encoding the GAG, the tyrosine recombinase (YR) and the pol regions (Reverse transcriptase (RT)/RnaseH (RH)/MethylTransferase (MT) domain series) correspond to shaded boxes. B. Positions of the degenerated primers defined in this study along the DIRS1-like pol region. Three types of primers are represented: in grey bold, the GD primers that correspond to conserved motifs of Ty3/gypsy-like retrotransposons, also shared with DIRS1-like elements; in black bold, the DD primers that correspond to conserved motifs specific to DIRS1-like elements and underlined, the non degenerate primer Retro1+ that spans the highly well-conserved YLDD motif that is present in both LTR retrotransposons and DIRS-like elements. For each primer, the orientation (arrow) and the corresponding conserved motif (uppercase) are indicated.
Figure 2
Figure 2
Nucleotide sequence identity matrix of the Alvi1 to Alvi5 families. The matrix is built using the pairwise deletion of gaps option included in the MEGA4.1 software. Results of intra-family computation are given in black bold. For each intra or inter-families observation, the mean of DNA identity is indicated as well as the lowest and highest (Min/Max) values represented in italics. The number of sequences included in each Alvi family is also noted.
Figure 3
Figure 3
Unrooted phenetic tree based on nucleotide DIRS1-like sequences identified in hydrothermal organisms. The tree was constructed using Neighbor Joining method and pairwise deletion of gaps option included in MEGA4.1 software. Alvi1-5 families are originated from hydrothermal shrimps and Ymur1-3 elements were identified in Munidopsis recta. Support for individual clades was evaluated using non-parametric bootstrapping obtained from 1000 bootstrap replicates. Only bootstrap nodes value over 70% are indicated. Distances were calculated with Tamura 3 parameter model plus gamma distribution's correction for nucleotides.
Figure 4
Figure 4
Species distribution of the different DIRS1-like families. Names of the diverse TEs analyzed are shown on top. Plus and minus signs indicate the presence (+) or absence (-) of these elements in the different species tested. Genetic relationships between species and infraorders are represented by a tree topology, reconstructed from previous studies [27,36,62,66], with hydrothermal vent species indicated in purple. Position of Maja squinado within Brachyura is still unresolved, this species was thus arbitrarily placed at the base of the infraorder. * The Ynno1 family of astacideans has been also detected in an EST database from another lobster species (H. americanus).
Figure 5
Figure 5
Rooted phylogenic tree based on RT/RH amino acid sequences of DIRS1-like retrotransposons. Tree performed on a core data set including representative amino acid consensus sequences of the RT/RH domains of the Ymur3 and Alvi1-5 families and 16 previously well-described DIRS1-like retrotransposons (see Table 1 for accession numbers). PAT-like sequences were used as outgroup as well as Ty3/gypsy-like elements according to the close phylogenic relationships of their RT/RH domains with those of DIRS-like retrotransposons: Clonorchis sinensis CsRn1, [GenBank:AAK07485]; Drosophila melanogaster 412, [GenBank:CAA27750.1]; Tetraodon nigroviridis TnGr1 available on Retrobase database [50];Takifugu rubripes sushi-ichi, [GenBank:AAC33526]; Caenorhabditis briggsae CbPAT1, [GenBank:XP_001664700.1] and Strongylocentrotus purpuratus SpPAT1 available on Retrobase database [50]. The tree was constructed using the Maximum Likelihood method and 100 bootstrap replicates. Only nodes with bootstrap value over 50% are indicated. Distances were calculated using WAG model with gamma distribution's correction for amino acids. The two previously described clades [41,48], DrDIRS1-clade and TcDIRS1-clade, are indicated.

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