Horizontal transfers of Mariner transposons between mammals and insects
© Oliveira et al.; licensee BioMed Central Ltd. 2012
Received: 11 May 2012
Accepted: 24 August 2012
Published: 26 September 2012
Active transposable elements (TEs) can be passed between genomes of different species by horizontal transfer (HT). This may help them to avoid vertical extinction due to elimination by natural selection or silencing. HT is relatively frequent within eukaryotic taxa, but rare between distant species.
Closely related Mariner-type DNA transposon families, collectively named as Mariner-1_Tbel families, are present in the genomes of two ants and two mammalian genomes. Consensus sequences of the four families show pairwise identities greater than 95%. In addition, mammalian Mariner1_BT family shows a close evolutionary relationship with some insect Mariner families. Mammalian Mariner1_BT type sequences are present only in species from three groups including ruminants, tooth whales (Odontoceti), and New World leaf-nosed bats (Phyllostomidae).
Horizontal transfer accounts for the presence of Mariner_Tbel and Mariner1_BT families in mammals. Mariner_Tbel family was introduced into hedgehog and tree shrew genomes approximately 100 to 69 million years ago (MYA). Most likely, these TE families were transferred from insects to mammals, but details of the transfer remain unknown.
KeywordsDNA transposon Genome evolution Horizontal transfer Mariner
In contrast to the vertical transmission of the genetic material from parents to offspring, the horizontal transfer (HT) is a process in which new genetic information is transmitted between different, sometimes distant, species[1, 2]. HT is likely to be one of the factors leading to the persistence of transposable elements (TEs) in eukaryotes[3–5], and complicating the evolutionary trees.
The detection of HT is mostly inferential, mainly based on the combination of two types of evidence: unusually high similarity between TE sequences from species that have long diverged from each other, and a limited distribution of one particular TE family within a group of species. To date, numerous HTs have been detected in eukaryotes[6–10], but of particular interest are HTs across distant branches. A recent example of such a rare event is HT of hAT DNA transposon families between vertebrate and invertebrate species.
Pairwise identities (%) between the Mariner_Tbel consensus from mammals ( Tupaia belangeri , Erinaceus europaeus ) and insects ( Pogonomyrmex barbatus , Harpegnathos saltator )
Divergence of Mariner transposable element (TE) families in mammalian and insect genomes
15.0 ± 2 (183)
19.4 ± 3 (34)
6.3 ± 1 (53)
7.2 ± 2 (16)
21.2 ± 2 (27)
28.0 ± 3 (25)
17.3 ± 2 (102)
12.1 ± 1 (159)
20.1 ± 3 (12)
14.7 ± 2 (95)
7.6 ± 1 (101)
In the ant genomes, no Mariner family was yet identified as unambiguously present in the common ancestor of all ant species. Among potential candidates are the oldest known Mariner families present in some of the ant genomes (for example, Mariner-28_SIn or Mariner-94_HSal; Figure1). These small families may have expanded in the common ancestor of all ant species (140 MYA), assuming that they were lost in some ant species. Alternatively, these old families might have expanded in some ant species after they split from their common ancestor. Under either scenario, the outermost ages when the two ant Mariner_Tbel families expanded could be still estimated by comparing their diversities with the diversity of Mariner-28_SIn (Table2). Based on that, Mariner_Tbel family in the red harvester ant (P. barbatus) and Jerdon's jumping ant (H. saltator) expanded at most approximately 43 and approximately 50 million years ago, respectively.
The above age estimates suggest that the two ant Mariner_Tbel families are possibly younger than the mammalian Mariner_Tbel families. However, the history of Mariner_Tbel can be traced further back in ants and their insect relatives than in mammals. Individual Mariner_Tbel-like elements from distinct families, such as AEAQ01009575, AEAB01001421 and AFJA01006902 (Figure1B), were also found in the genomes of two other ants (Solenopsis invicta and Camponotus floridanus) as well as in the alfalfa leafcutting bee (Megachile rotundata). These Mariner_Tbel-like sequences and Mariner_Tbel sequences form a single lineage in the phylogenetic tree (Figure1B), with the bee sequences in a more ancestral position (Figure1B). The topology of this particular lineage mirrors the evolutionary history of the ant and bee species (Figure1A). Furthermore, Figure1B indicates that the Mariner_Tbel family and many other similar Mariner families in ants and other insects shared a common ancestral sequence. These observations suggest the ancestor of ants Mariner_Tbel may have been present in some ant or other insect species very long time ago, probably as far back as the common ancestor of bees and ants (approximately 150 MYA). Thus, the mammalian Mariner_Tbel families probably originated from HTs from insects to mammals through some unknown vectors. Given that the two mammals belong to two distinct lineages, Mariner_Tbel in tree shrew and hedgehog may represent two independent HTs (Figure1A). Notably, we cannot rule out the possibility that the Mariner_Tbel families in one of the two ant species, or both, also originated by HTs. This possibility is suggested by two facts: (a) the relatively young ages (at most approximately 43 to 50 MYA) of the two families, (b) the high identity (98.5%) between the two family consensus sequences, even H. saltator and P. barbatus diverged from each other approximately 100 million years ago. Among insect species, frequent HTs have been documented in flies. Alternatively, Mariner_Tbel sequences could have survived for a very long time in either of the two ant genomes before the most recent family expansions.
Mariner1_BT sequences detected in mammals
Muntiacus muntjak vaginalis
Remarkably, the other closest relatives of Mariner1_BT are all found in ant species: Mariner1_BT coclusters significantly (bootstrap = 83) with three other ant Mariner families (Mariner-5_ACe, Mariner-28_SIn and Mariner-35_HSal) (Figure1B). Given the vast diversity of Mariners found in insects (Figure1B), and the confined distribution of Mariner1_BT in mammals, we propose Mariner1_BT family could also originate from a horizontally transferred insect-like element. Using a similar method above, that is, based on the family divergence and mammalian phylogeny (Table2 and Figure1A), we estimated the ages of bovine Mariner1_BT to be 90 to 85 MYA, and 90 to 63 MYA for dophin T. truncatus Mariner1_BT family. The age of Mariner1_BT in bat could not be estimated due to insufficient data. We also could not determine if HT happened in mammals more than once, because the three taxonomic groups that include Mariner1_BT are relatively close.
In summary, this is the first report of two cases of horizontally transferred Mariner elements (Mariner_Tbel and Mariner1_BT) between insects and mammals. Previously, four families of DNA transposons from the hAT superfamily were also found to be involved in multiple waves of HT between insects and other vertebrates including mammals. This could partially be attributed to the fact that insects are the largest and the most diverse group of invertebrate animals on earth. While insects are the most likely source of the horizontally transferred transposons, the original source or possible intermediaries, such as parasitic insects or viruses, remain unclear. This is complicated by the possibility that recurrent HTs of related Mariner elements are likely to take place between different insects. The role of viruses in HT proposed some time ago still remains to be understood. As more genome sequence data become available, more mechanistic details on HT between mammals and insects are likely to emerge.
Mariner transposable elements from Repbase (http://www.girinst.org/repbase/) were used as an initial query to screen Mariners in diverse genomes available at NCBI (National Center for Biotechnology Information:http://www.ncbi.nlm.nih.gov/). Family consensus sequences were constructed whenever possible. The copy numbers in each family were determined by BLASTN using consensus sequences as queries. Sequence divergence within each family was assessed by the average pairwise k-distance (Kimura two-parameter model) between individual insertions and the corresponding consensus sequences. The k-distance was calculated using the software MEGA 4. For a given family, individual sequences used in k-distance calculation were randomly chosen from the family members; in most cases individual sequences matched >70% of the consensus length.
We used Mariner_Tbel and Mariner1_BT as BLASTN queries against Repbase to select top scoring TE entries for phylogeny analysis. Individual sequences selected from GenBank were also used in the tree if Repbase consensus sequences were not available. The sequence alignments are shown in Additional file1. The alignments were done using the online MAFFT server (http://mafft.cbrc.jp/alignment/software/). The phylogeny tree was inferred using MEGA 4, using the neighbor joining (NJ) method and k-distances. Branch support was estimated using 1,000 bootstrap replicates.
This work was supported by funds from the Sao Paulo Research Foundation (FAPESP), Sao Paulo State University (UNESP) and the National Institutes of Health grant 5 P41 LM006252. The content of this manuscript is solely the responsibility of the authors and does not necessarily represent the official views of the National Library of Medicine or the National Institutes of Health.
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