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Repeated Horizontal Transfers of Four DNA Transposons in Invertebrates and Bats Zhou Tang1†, Hua-Hao Zhang2†, Ke Huang3, Xiao-Gu Zhang2, Min-Jin Han1 and Ze Zhang1*

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Repeated Horizontal Transfers of Four DNA Transposons in Invertebrates and Bats Zhou Tang1†, Hua-Hao Zhang2†, Ke Huang3, Xiao-Gu Zhang2, Min-Jin Han1 and Ze Zhang1* Tang et al. Mobile DNA (2015) 6:3 DOI 10.1186/s13100-014-0033-1 RESEARCH Open Access Repeated horizontal transfers of four DNA transposons in invertebrates and bats Zhou Tang1†, Hua-Hao Zhang2†, Ke Huang3, Xiao-Gu Zhang2, Min-Jin Han1 and Ze Zhang1* Abstract Background: Horizontal transfer (HT) of transposable elements (TEs) into a new genome is considered as an important force to drive genome variation and biological innovation. However, most of the HT of DNA transposons previously described occurred between closely related species or insects. Results: In this study, we carried out a detailed analysis of four DNA transposons, which were found in the first sequenced twisted-wing parasite, Mengenilla moldrzyki. Through the homology-based strategy, these transposons were also identified in other insects, freshwater planarian, hydrozoans, and bats. The phylogenetic distribution of these transposons was discontinuous, and they showed extremely high sequence identities (>87%) over their entire length in spite of their hosts diverging more than 300 million years ago (Mya). Additionally, phylogenies and comparisons of transposons versus orthologous gene identities demonstrated that these transposons have transferred into their hosts by independent HTs. Conclusions: Here, we provided the first documented example of HT of CACTA transposons, which have been so far extensively studied in plants. Our results demonstrated that bats had continuously acquired new DNA elements via HT. This implies that predation on a large quantity of insects might increase bat exposure to HT. In addition, parasite-host interaction might facilitate exchanging of their genetic materials. Keywords: Horizontal transfer, CACTA transposons, Mammals, Recent activity Background or isolated species. HT of a transposon into a new gen- DNA-mediated or class 2 transposons were one class of ome allows the element to evade inevitable extinction, transposable elements (TEs). Most DNA transposons suggesting that HT plays important roles in the persist- transpose via a ‘cut and paste’ mechanism implemented ence of TEs [4]. In addition, HT of TEs into a new by transposases. They were generally characterized by genome is also regarded as important forces to drive terminal inverted repeats (TIRs) and target site duplica- genome variation and biological innovation. tion (TSD) [1]. Based on their transposases, DNA transpo- Generally, there are three criteria used to infer HT sons could be classified into 19 superfamilies, including events: (1) high sequence similarity of TEs from divergent Tc1/mariner, hAT, PiggyBac, CACTA, MuDR, Merlin, taxa, (2) incongruence between TE and host phylogeny, Transib, P, PIF/Harbinger, Mirage, Zator, Ginger, Kolobok, and (3) a patchy TE distribution within a group of taxa Chapaev, Novosib, Rehavkus, PHIS, Sola,andAcadem [7,8]. The first documented example of HT of TEs was [2,3]. the P element of Drosophila [9]. More than 330 cases Although the possibility of stochastic loss suggests that (188 cases for DNA transposons and 142 cases for RNA TEs should be a seemingly inevitable vertical extinction transposons) of eukaryote-to-eukaryote HT events of TEs in their original host genomes, TEs are widespread in or- were described so far [10]. However, no documented ganisms [1,4-6]. Horizontal transfer (HT) is a process of example of HT has been described for the CACTA super- genetic material exchanging among non-mating species family of DNA transposons, which so far has extensively been studied in plants [6,11]. In addition, most of HT of * Correspondence: [email protected] DNA transposons (122 out of 188) previously described † Equal contributors occurred between closely related species or insects [10]. 1School of Life Sciences, Chongqing University, Chongqing 400044, China Full list of author information is available at the end of the article © 2015 Tang et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Tang et al. Mobile DNA (2015) 6:3 Page 2 of 10 In this study, we described four DNA transposons which and 2). These four DNA transposons formed the start were present in diverse invertebrate and vertebrate ani- pointing of this study. They were grouped into hAT, mals. The combination of high identity levels between CACTA,andpiggyBac superfamilies based on their TEs despite deep divergence times of their host taxa, similarities to known members of these superfamilies patchy TE taxonomic distribution, and lower genetic dis- (Table 1). Full-length or partial ancestral sequences in tances for TEs than for host genes clearly demonstrated each species were reconstructed and compared to each that they had horizontally transferred into their hosts. other (Additional file 1: Table S1). The first DNA transposon, called Buster1, was found in Results M. moldrzyki, Schmidtea mediterranea, Rhodnius prolixus, Distribution patterns of four DNA transposons and Heliconius melpomene (Table 1 and Figure 2). Except The twisted-wing parasite, Mengenilla moldrzyki, is the for H. melpomene, this element in other three species gen- first sequenced species of Strepsiptera [12]. Nineteen erated both autonomous and non-autonomous elements seventy potential TEs of the twisted-wing parasite were (including miniature inverted-repeat transposable elements downloaded from Dryad Digital Repository (http://data- (MITEs)). Multiple alignments of MITEs and its autono- dryad.org/resource/doi:10.5061/dryad.ts058.2). The screen- mous ancestors indicated that they originated by internal ing of the distribution of these transposons revealed that deletions from master elements. These results supported four of these 1970 TEs yielded highly significant (>87%) hits the hypothesis that MITEs borrowed the machinery of au- in many diverse species, not only in insects but also in tonomous DNA transposons to transpose [1]. Insertion bias freshwater planarian, hydrozoans, or bats (Table 1, Figures 1 and phylogenetic analysis demonstrated that they belonged Table 1 Characteristics of four DNA transposons in this study Superfamily Family Organism TEs Length Copy TIRs (5′-3′) Average References (bp) no. divergence ± SE hAT Buster1 Schmidtea Buster1_SM 2,463 17 CAGGGCTTCTTAAAC 8.22 ± 5.66 hAT-11_SM[13] mediterranea Buster1_NA1_SM 373 270 CAGGGCTTCTTAAAC 1.45 ± 0.65 This study Buster1_NA2_SM 449 31 CAGGGCTTCTTAAAC 1.45 ± 0.75 This study Mengenilla Buster1_MM 2,196 3 ND 2.16 ± 3.75 This study moldrzyki Buster1_NA1_MM 366 44 CAGGCCTTCTTAAACT 9.94 ± 2.83 This study Rhodnius prolixus Buster1_RP 2,281 3 ND 0.86 ± 1.49 This study Buster1_NA1_RP 580 17 CAGGGCTTCTTAAACT 1.82 ± 0.85 This study Heliconius Buster1_NA1_HM 500 42 CAGGGTTTCTTAAACT 2.32 ± 1.38 nhat-10_Hmel[13] melpomene Buster2 M. moldrzyki Buster2_NA1_MM 365 252 CAACGGTGGCCA 13.5 ± 2.16 This study R. prolixus Buster2 _NA1_RP 908 16 CAGGGGGGGGCCAACCT 4.74 ± 1.51 This study Nycticeius Buster2 _NA1_NH 337 >10 CAGGGGTGGCCAACCT 4.81 ± 1.48 nhAT-5a_Nhu humeralis [unpublished] Buster2_NA2_NH 246 >104 CAGGGGTGGCCAACCT 4.63 ± 1.87 nhAT-2a_Nhu [unpublished] CACTA Spongebob M. moldrzyki Spongebob_NA1_MM 496 40 ND 9.88 ± 3.95 This study R. prolixus Spongebob_NA1_RP 433 2 ND 2.74 ± 3.87 This study Bombyx mori Spongebob_NA1_BM 468 17 ND 10.6 ± 3.69 This study Hydra Spongebob_ HMa 5,836 441 CCCAGCCAACATT 5.94 ± 3.48 EnSpm-4N1_HM[2] magnipapillata GAC (17) piggyBac Kenshin M. moldrzyki Kenshin_MM 2,244 15 CACTAGA 13.2 ± 5.49 This study Megachile Kenshin_MR 2,520 9 CACTAGA 9.91 ± 3.84 This study rotundata Kenshin_NA1_MR 235 46 CACTAGA 2.82 ± 2.24 This study Myotis davidii Kenshin_MD 2,108 1 CACTAG ND This study Kenshin_NA1_MD 1,267 23 CACTAGA 2.16 ± 0.60 This study Kenshin_NA2_MD 627 3 CACTAGA 2.46 ± 0.20 This study Tang et al. Mobile DNA (2015) 6:3 Page 3 of 10 Figure 1 Diagram showing the detail information about transposons of Buster1 (A), Buster2 (B), Spongebob (C), and Kenshin (D). Black triangles represent the TIRs. Gray rectangles represent non-coding regions, and purple rectangles indicate transposase regions. Percentages of identity were calculated using Bioedit. Blue regions represent the variable area of transposons. Tang et al. Mobile DNA (2015) 6:3 Page 4 of 10 Figure 2 The taxonomic distribution of Buster1, Buster2, Spongebob,andKenshin among species for which genome sequences are available. Presence of these transposon families in each lineage are denoted by plus sign. Species divergence is taken from previous literatures [14-17]. Tang et al. Mobile DNA (2015) 6:3 Page 5 of 10 to one member of the Buster family of the hAT superfam- ancestral element. Buster1 was found in low copy number ily (Figures 3A and 4A). Structure analysis indicated (<50) in most species, except for the freshwater planarian that the subterminal regions of the elements contain Schmidtea mediterranea (Buster1_NA1_SM)wherethis TGGGTCGCG tandem repeats. Generally, short repeats element was found more than 250 copies (Table 1). The in subterminal regions have been used to distinguish average sequence divergence between Buster1_NA1_SM different hAT transposons [18]. Thus, Buster1 might copies and its consensus sequence was only 1.45%, indi- represent
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