Horizontal transfer of transposons between and within crustaceans and insects
© Dupeyron et al.; licensee BioMed Central Ltd. 2014
Received: 11 October 2013
Accepted: 6 January 2014
Published: 29 January 2014
Horizontal transfer of transposable elements (HTT) is increasingly appreciated as an important source of genome and species evolution in eukaryotes. However, our understanding of HTT dynamics is still poor in eukaryotes because the diversity of species for which whole genome sequences are available is biased and does not reflect the global eukaryote diversity.
In this study we characterized two Mariner transposable elements (TEs) in the genome of several terrestrial crustacean isopods, a group of animals particularly underrepresented in genome databases. The two elements have a patchy distribution in the arthropod tree and they are highly similar (>93% over the entire length of the element) to insect TEs (Diptera and Hymenoptera), some of which were previously described in Ceratitis rosa (Crmar2) and Drosophila biarmipes (Mariner-5_Dbi). In addition, phylogenetic analyses and comparisons of TE versus orthologous gene distances at various phylogenetic levels revealed that the taxonomic distribution of the two elements is incompatible with vertical inheritance.
We conclude that the two Mariner TEs each underwent at least three HTT events. Both elements were transferred once between isopod crustaceans and insects and at least once between isopod crustacean species. Crmar2 was also transferred between tephritid and drosophilid flies and Mariner-5 underwent HT between hymenopterans and dipterans. We demonstrate that these various HTTs took place recently (most likely within the last 3 million years), and propose iridoviruses and/or Wolbachia endosymbionts as potential vectors of these transfers.
KeywordsHorizontal transfer Transposable elements Isopod crustaceans Hexapods
Horizontal transfer (HT) of genetic material is the transmission of DNA between non-mating organisms . Most known eukaryote-to-eukaryote HT events are transfers of transposable elements (TEs) . Given the profound impact TEs have on the genome architecture of their hosts, HT of TEs (HTT) is increasingly recognized as an important force in eukaryote genome evolution . On the TE side, spreading between genomes via HT may be viewed as a strategy to escape vertical extinction due to purifying selection, mutational decay and/or host defense mechanisms. Among the over 330 cases of eukaryote-to-eukaryote HTT events characterized so far, the vast majority involve DNA transposons (n = 188 cases) and LTR retrotransposons (n = 118 cases) , indicating that the long-term survival of these TEs may rely more on HT than that of non-LTR retrotransposons. Yet, while whole genomes are sequenced at an exponential pace, the global diversity of eukaryote genomes is still poorly represented, precluding any strong generalization on HTT dynamics. Even in animals, whole genome sequencing efforts are biased towards species closely related to model organisms or species of economic interest, and whole genome sequences are lacking for many large taxonomic groups. Our current understanding of the global HTT dynamics and impacts is therefore incomplete, both at the host and TE level.
With only one genome fully sequenced  out of over 50,000 species described , crustaceans are particularly underrepresented in genome databases. The order Isopoda (Vericrustacea clade according to ) is unique among crustaceans in that the colonization of landmasses by one of its lineages (belonging to the suborder Oniscidea) during the Mesozoic yielded a large diversity of terrestrial species (>3,600 ) now distributed all over the world in every biotope (except for the poles) . In this study we report new cases of HTT involving terrestrial isopod crustaceans and hexapods. We used a combination of cross-species PCR screening of TEs, phylogenetic and other evolutionary analyses to characterize in detail these HTT and to shed light on the evolutionary dynamics of the first two TEs described in isopod crustaceans.
Results and discussion
Characterization of two Mariner elements in the isopod crustacean Armadillidium vulgare
In order to detect TEs that underwent horizontal transfer between isopod crustaceans and other taxa, we used all consensus sequences deposited in Repbase  as of May 2013 as queries to perform BLASTn searches on draft genomic contigs and on a transcriptome of the pill bug Armadillidium vulgare that have been generated in our lab as part of other ongoing projects. Importantly, the contigs generated by these projects are too short to carry out a comprehensive de novo mining of A. vulgare TEs. The BLASTn searches yielded two TEs belonging to the Tc1/Mariner superfamily of Class II DNA transposons that show more than 90% identity over more than 500 bp to A. vulgare sequences. The first one (Crmar2) was originally characterized in the tephritid fly Ceratitis rosa based on a PCR/sequencing screening , and the second one (Mariner-5_Dbi) was described by Kojima and Jurka  in Drosophila biarmipes based on whole genome sequence data mining. We reconstructed an A. vulgare consensus sequence of both elements (named Crmar2_Avul and Mariner-5_Avul) using 100 to 1300 bp-long fragments resulting from our various BLAST outputs, such that the entire sequence of the consensus was covered by at least five different copies. Crmar2_Avul is 1304 bp in length, has 39-bp terminal inverted repeats (TIRs) and encodes a 361 amino acid (aa) transposase while Mariner-5_Avul is 1013 bp in length, has 28-bp TIRs and encodes a 200 aa transposase. Both elements are flanked by TA target site duplications, which is characteristic of the Tc1/Mariner superfamily . The evolution of this superfamily has yielded a large number of elements which have colonized the genome of many eukaryote taxa [14, 15] and have been classified in various subfamilies (for example, ). Crmar2 belongs to the rosa subfamily  and our phylogenetic analysis of the transposase revealed that Mariner-5_Dbi belongs to the irritans subfamily [see Additional file 1: Figure S1].
Taxonomic distribution of the two Mariner elements in eukaryotes
Horizontal transfer of the two Mariner elements between hexapods and isopods and within hexapods
Recent horizontal transfer of the two Mariner elements within isopods
To provide an estimate of the absolute age of the activity burst of Mariner-5 and Crmar2, we divided the average copy/consensus distance calculated for each element in D. biarmipes (11%) and D. bipectinata (6.9%) by the experimentally derived neutral substitution rate of D. melanogaster (0.0346 substitutions per base per million years (myr); [24–26]). This yielded a burst age of 3.2 myrs for Mariner-5 in D. biarmipes and 2 myrs for Crmar2 in D. bipectinata. The age of Mariner-5_Avul and Crmar2_Avul cannot be precisely estimated because nuclear substitution rates are not available for isopods. Together with the absence of shared orthologous copies of both elements between the various isopods species and the seemingly polymorphic state of Crmar2 in A. vulgare, the fact that an intact Crmar2_Avul transposase is transcribed in this species is consistent with a recent invasion of isopod genomes by Mariner-5_Avul and Crmar2_Avul and suggest both elements are active sources of genomic variation in this major crustacean group. In addition, given that isopod Crmar2 and Mariner-5 are highly similar to Drosophila Crmar2 and Mariner-5 (95% and 93% identity, respectively; Figure 2), we believe these HTTs most likely took place within the past few million years at most.
Number of horizontal transfer of transposon events
Potential vectors of horizontal transfer
Though the question of the mechanisms and vectors underlying HTT between multicellular eukaryotes remains largely open, growing evidence suggests that host-parasite relationships likely facilitate such transfers [27–31]. In particular, viruses are often cited as ideal HTT vectors due to their capacity to inject DNA/RNA into host cells [32–35]. Though the viral fauna infecting the various species involved in Crmar2 and Mariner-5 HTT is poorly known, it is noteworthy that members of the Iridoviridae have been found in several species of dipterans, hymenopterans and terrestrial isopods [36, 37]. In addition, a recent study identified two TEs inserted in the genome of an iridovirus infecting dipteran , emphasizing the potential of this type of viruses to shuttle transposons between their hosts. Another possible route for HTT to occur in arthropods is via transfers of endosymbiotic bacteria. Several species of isopods as well as D. ananassae, D. bipectinata and A. suspensa are known to bear intracellular, maternally transmitted alphaproteobacteria called Wolbachia[39–43]. The fact that isopod Wolbachia strains are known to have undergone several HT  and that several genes of eukaryotic origin have been found integrated in Wolbachia genomes [45–47] suggest that endosymbionts could also facilitate HT of DNA between hosts.
In this study, we have characterized the evolutionary dynamics of two Tc1/Mariner elements in isopod crustaceans and shown that their current taxonomic distribution in arthropods results from at least one HT between hexapods and isopods as well as one or more HTs within isopods. Furthermore, we have demonstrated that Crmar2 transferred horizontally between drosophilid and tephritid flies and that Mariner-5 underwent HT between Diptera and Hymenoptera. Conservatively, and assuming that Crmar2 and Mariner-5 transferred horizontally only once within the isopods, we have uncovered a total of six new HTT events in this study. Together with 70 previously known cases (for example, [48–50]; reviewed in ) our results bring to 76 the number of HT events described in metazoans for the Tc1/Mariner superfamily, further emphasizing the indifference of these elements to host factors to transpose . Of note, HT of two other Mariner elements have previously been characterized in marine crustaceans  (one between two decapods and one between a decapod and an amphipod), but our study is the first to report HTT involving terrestrial crustaceans. Finally, we have shown that these newly described HTT events most likely took place within the last 3 myrs, and we propose iridoviruses and/or Wolbachia endosymbionts as the potential vectors of transfer, a hypothesis that will be interesting to test in future studies.
Mining of available eukaryote genomes
In order to identify transposable elements similar to Crmar2 and Mariner-5_Dbi that could have been horizontally transferred between isopods and other taxa we used the nucleotide sequence of the two elements to carry out BLASTn searches against the nr (non-redundant nucleotide), EST (expressed sequence tag) and WGS (whole genome sequence) databases available on the NCBI website. We considered only those elements that showed more than 90% nucleotide identity over more than 500 bp of our query sequences.
DNA extraction, PCR, cloning, and sequencing
Genomic DNA was extracted from 14 species of terrestrial isopods (Figure 3) using the Qiagen™ DNeasy blood and tissue extraction kit (Hilden, Germany). PCRs were carried out using four types of primer pairs: 1) one pair designed on the internal region of Mariner-5_Avul and Crmar2_Avul, 2) three and four pairs designed to screen specific copies of the two elements at orthologous position in the 14 isopod species, 3) one pair designed to amplify the mitochondrial cytochrome oxidase I (Co1) for the six species for which this gene is not available in Genbank, and 4) one pair designed to amplify the mitochondrial 16S gene for all species included in this study except for T. pusillus (taken from Genbank). The list of PCR primers used in this study, together with their respective melting temperatures, is given in Additional file 5: Table S1. PCR reactions were conducted using the following temperature cycling: initial denaturation at 94°C for 5 min, followed by 30 cycles of denaturation at 94°C for 30 s, annealing at 52 to 58°C (depending on the primer pair) for 30 s, and elongation at 72°C for 45 sec, ending with a 10 min elongation step at 72°C. PCR products obtained with the Co1 primers were purified and directly sequenced using ABI BigDye sequencing mix (1.4 μl template PCR product, 0.4 μl BigDye, 2 μl manufacturer supplied buffer, 0.3 μl primer, and 6 μl H2O). Sequencing reactions were ethanol precipitated and run on an ABI 3730 sequencer. PCR products obtained with the primers internal to Crmar2_Avul and Mariner-5_Avul were cloned into pGEM-T easy vector (Promega, USA, Madison, WI) and several clones were Sanger-sequenced as described above until we obtained five different copies of each element in the various species in which we found them.
Sequencing of androgenic gland hormone (Agh) cDNA
Total RNA was isolated from androgenic glands of fifteen males (6 glands per individual) using the RNeasy Mini kit (Qiagen, Hilden, Germany). The cDNA was synthesized using the M-MLV-RT kit (Promega). PCR amplification was performed using several degenerated primer pairs designed on the consensus sequences of Agh cDNAs of A. vulgare, P. scaber and P.dilatatus [see Additional file 6: Table S2] . PCR and direct sequencing were performed as described above.
The expression of Crmar2_Avul and Mariner-5_Avul was assessed in both dissected ovaries and somatic tissues (head + nervous chain) of A. vulgare females using the SuperScript™ III First-Strand Synthesis System for RT-PCR» (Invitrogen, Eugene, OR, USA).
Transposon distances versus gene distances
All Crmar2 and Mariner-5 consensus sequences reconstructed in this study are provided in Additional file 7: Dataset 2. In order to test whether Crmar2 and Mariner-5 TEs were inherited vertically or horizontally we compared the distances calculated between TE consensus sequences and between several orthologous genes for several pairs of taxa. To calculate gene distances between Isopoda and Hexapoda, we used the 57 A. vulgare genes sequenced by Regier et al.  as queries to perform BLASTn searches against the D. melanogaster genome. We chose the D. melanogaster genome rather than the genome of Drosophila species involved in the HTT characterized in this study because it is the most completely sequenced and best assembled Drosophila genome available. We found 46 A. vulgare orthologs in D. melanogaster, which we aligned at the nucleotide level between the two species. For the Ceratitis/Drosophila gene distances we used the 46 genes resulting from the above search as queries to perform BLASTn searches against the whole genome sequence of C. capitata. This search yielded 41 genes that we aligned at the nucleotide level with those of D. melanogaster. The same approach was used to find genes orthologous between D. melanogaster and H. saltator which resulted in the alignment of 37 genes. Genetic distances between Crmar2 and Mariner-5 consensus sequences as well as between each pair of orthologous genes were calculated using the Jukes Cantor model in MEGA 5 . The name of all genes and the distances between them are provided in Additional file 8: Table S3. Jukes Cantor distances were also calculated between the various copies of both TEs found within each genome in which we found them.
The phylogeny of the 14 terrestrial isopod species understudy was reconstructed using 16S, Co1, and Agh sequences. All sequences produced in this study were deposited in Genbank under accession numbers KF957774-KF957833. Each gene was aligned manually using BioEdit 126.96.36.199 , and ambiguous regions were removed. All alignments are provided in Additional file 9: Dataset 3. A bootstrapped neighbor joining phylogeny was first reconstructed using MEGA 5 for each alignment with the maximum likelihood distance option. Given that no incongruence supported by bootstrap values >50% was observed between the three resulting trees (not shown), we then concatenated the three alignments and reconstructed a bootstrapped maximum likelihood phylogeny of the three combined markers using PhyML 3 . A bayesian analysis of this alignment was also performed using MrBayes  in order to obtain posterior probabilities for each node of the tree. The model of nucleotide evolution best fitting the combined alignment (GTR + I + G) and used for the phylogenetic analyses was chosen based on the Akaike information criterion (AIC) in jModeltest 2 .
The phylogeny of Crmar2 and Mariner-5 was reconstructed based on alignments of all different copies of each element from each species in which we found them. Ambiguous regions and regions absent in more than 25% of the sequences were removed. Alignments are provided in Additional file 9: Dataset 3. The model of nucleotide evolution best fitting each alignment (TPM1uf + G for both elements) was chosen based on the Akaike information criterion (AIC) in jModeltest 2 and each alignment was analyzed using PhyML 3. In order to assess the phylogenetic position of Mariner-5_Dbi in the mariner tree, we have aligned the amino acid sequence of a transposase representative of most described mariner subfamily and performed a neighbor joining analysis using MEGA 5 (JTT model, 1000 bootstrap replicates). The accession numbers of the sequences we have used are provided in Additional file 1: Figure S1.
horizontal transfer of transposons
long terminal repeat
reverse-transcription polymerase chain reaction
We thank all the technical staff of the UMR CNRS 7267. We acknowledge Catherine Debenest for assistance with the dissection of terrestrial isopods and Richard Cordaux and Pierre Grève for insightful comments on an earlier version of the manuscript. This work was supported by the CNRS, the Agence Nationale de la Recherche (ANR ImmunSymbArt 10-BLAN-1701), and a European Research Council Starting Grant (FP7/2007-2013, grant 260729 EndoSexDet) to Richard Cordaux.
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