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Next-generation sequencing reveals recent horizontal transfer of a DNA transposon between divergent mosquitoes.

Diao Y, Qi Y, Ma Y, Xia A, Sharakhov I, Chen X, Biedler J, Ling E, Tu ZJ - PLoS ONE (2011)

Bottom Line: Among 24 mosquito species surveyed, MJ1 is only found in Ae. aegypti and the hyrcanus group of anopheline mosquitoes to which An. sinensis belongs.Therefore we have shown that it is feasible to use low coverage sequencing to systematically uncover horizontal transfer events.Expanding such efforts across a wide range of species will generate novel insights into the relative frequency of horizontal transfer of different TEs and provide the evolutionary context of these lateral transfer events.

View Article: PubMed Central - PubMed

Affiliation: Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, Shanghai, China.

ABSTRACT
Horizontal transfer of genetic material between complex organisms often involves transposable elements (TEs). For example, a DNA transposon mariner has been shown to undergo horizontal transfer between different orders of insects and between different phyla of animals. Here we report the discovery and characterization of an ITmD37D transposon, MJ1, in Anopheles sinensis. We show that some MJ1 elements in Aedes aegypti and An. sinensis contain intact open reading frames and share nearly 99% nucleotide identity over the entire transposon, which is unexpectedly high given that these two genera had diverged 145-200 million years ago. Chromosomal hybridization and TE-display showed that MJ1 copy number is low in An. sinensis. Among 24 mosquito species surveyed, MJ1 is only found in Ae. aegypti and the hyrcanus group of anopheline mosquitoes to which An. sinensis belongs. Phylogenetic analysis is consistent with horizontal transfer and provides the basis for inference of its timing and direction. Although report of horizontal transfer of DNA transposons between higher eukaryotes is accumulating, our analysis is one of a small number of cases in which horizontal transfer of nearly identical TEs among highly divergent species has been thoroughly investigated and strongly supported. Horizontal transfer involving mosquitoes is of particular interest because there are ongoing investigations of the possibility of spreading pathogen-resistant genes into mosquito populations to control malaria and other infectious diseases. The initial indication of horizontal transfer of MJ1 came from comparisons between a 0.4x coverage An. sinensis 454 sequence database and available TEs in mosquito genomes. Therefore we have shown that it is feasible to use low coverage sequencing to systematically uncover horizontal transfer events. Expanding such efforts across a wide range of species will generate novel insights into the relative frequency of horizontal transfer of different TEs and provide the evolutionary context of these lateral transfer events.

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MJ1 schematic and sequence comparison.A) MJ1 schematic drawn according to the MJ1 consensus from Ae. aegypti. The schematic shows terminal inverted repeats (open arrows at the termini), an open reading frame (black bar with the start and end positions marked), and the relative positions of the catalytic triad, which is comprised of three aspartic acid (D) residues. B) Comparison of MJ1 sequences from Ae. aegypti and An. sinensis. Only variable sites are shown between the Aae_MJ1 consensus and Asi_MJ1_Clone1, a representative of Asi_MJ1 from An. sinensis. A one-base insertion between positions 1246 and 1247 in An. sinensis is not shown. The entire nucleotide sequences are shown in Supplemental Files S1 and S2.
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pone-0016743-g001: MJ1 schematic and sequence comparison.A) MJ1 schematic drawn according to the MJ1 consensus from Ae. aegypti. The schematic shows terminal inverted repeats (open arrows at the termini), an open reading frame (black bar with the start and end positions marked), and the relative positions of the catalytic triad, which is comprised of three aspartic acid (D) residues. B) Comparison of MJ1 sequences from Ae. aegypti and An. sinensis. Only variable sites are shown between the Aae_MJ1 consensus and Asi_MJ1_Clone1, a representative of Asi_MJ1 from An. sinensis. A one-base insertion between positions 1246 and 1247 in An. sinensis is not shown. The entire nucleotide sequences are shown in Supplemental Files S1 and S2.

Mentions: Full-length MJ1 sequences were independently obtained in two laboratories from two An. sinensis sources by PCR using the terminal inverted repeat as the primer, which anneal to both ends of MJ1. Nine clones were sequenced and all were confirmed to be An. sinensis MJ1 (Asi_MJ1). These nine clones were nearly identical to each other with some having a 19 nucleotide insertion. As shown in Figure 1, one Asi_MJ1 clone was 99% identical to the Aae_MJ1 consensus over the entire 1.3 kb element. The open reading frames of the two sequences encoded 379 amino acids, which showed >97% identity. Sequences of the Aae_MJ1 consensus and all nine genomic copies in Ae. aegypti are shown in Supplemental File S1 and sequences of the nine Asi_MJ1 clones are included in Supplemental File S2. Deduced peptide sequences of the Aae_MJ1 consensus and all individual MJ1 copies/clones that had intact open reading frames are included in Supplemental File S3. When individual MJ1 copies in Ae. aegypti were compared to individual MJ1 clones in An. sinensis at the nucleotide level, high sequence identities were observed, ranging from 97% to nearly 99%. Similar high identities were also observed at the amino acid level. For example, the Aae_MJ1 in CONTIG_13910, the only Ae. aegypti MJ1 copy that has an intact open reading frame, shares 97% amino acid identity with Asi_MJ1_Clone1. The fact that full-length MJ1 elements from Aedes and Anopheles mosquitoes are highly similar at both nucleotide and the amino acid levels indicates the possibility of horizontal transfer, considering that the two genera had diverged 145–200 million years ago [16]. In comparison, the range of amino acid identities between randomly selected orthologous gene products in Ae. aegypti and An. gambiae was from 28 to 96% with an average of 43% [18].


Next-generation sequencing reveals recent horizontal transfer of a DNA transposon between divergent mosquitoes.

Diao Y, Qi Y, Ma Y, Xia A, Sharakhov I, Chen X, Biedler J, Ling E, Tu ZJ - PLoS ONE (2011)

MJ1 schematic and sequence comparison.A) MJ1 schematic drawn according to the MJ1 consensus from Ae. aegypti. The schematic shows terminal inverted repeats (open arrows at the termini), an open reading frame (black bar with the start and end positions marked), and the relative positions of the catalytic triad, which is comprised of three aspartic acid (D) residues. B) Comparison of MJ1 sequences from Ae. aegypti and An. sinensis. Only variable sites are shown between the Aae_MJ1 consensus and Asi_MJ1_Clone1, a representative of Asi_MJ1 from An. sinensis. A one-base insertion between positions 1246 and 1247 in An. sinensis is not shown. The entire nucleotide sequences are shown in Supplemental Files S1 and S2.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3037385&req=5

pone-0016743-g001: MJ1 schematic and sequence comparison.A) MJ1 schematic drawn according to the MJ1 consensus from Ae. aegypti. The schematic shows terminal inverted repeats (open arrows at the termini), an open reading frame (black bar with the start and end positions marked), and the relative positions of the catalytic triad, which is comprised of three aspartic acid (D) residues. B) Comparison of MJ1 sequences from Ae. aegypti and An. sinensis. Only variable sites are shown between the Aae_MJ1 consensus and Asi_MJ1_Clone1, a representative of Asi_MJ1 from An. sinensis. A one-base insertion between positions 1246 and 1247 in An. sinensis is not shown. The entire nucleotide sequences are shown in Supplemental Files S1 and S2.
Mentions: Full-length MJ1 sequences were independently obtained in two laboratories from two An. sinensis sources by PCR using the terminal inverted repeat as the primer, which anneal to both ends of MJ1. Nine clones were sequenced and all were confirmed to be An. sinensis MJ1 (Asi_MJ1). These nine clones were nearly identical to each other with some having a 19 nucleotide insertion. As shown in Figure 1, one Asi_MJ1 clone was 99% identical to the Aae_MJ1 consensus over the entire 1.3 kb element. The open reading frames of the two sequences encoded 379 amino acids, which showed >97% identity. Sequences of the Aae_MJ1 consensus and all nine genomic copies in Ae. aegypti are shown in Supplemental File S1 and sequences of the nine Asi_MJ1 clones are included in Supplemental File S2. Deduced peptide sequences of the Aae_MJ1 consensus and all individual MJ1 copies/clones that had intact open reading frames are included in Supplemental File S3. When individual MJ1 copies in Ae. aegypti were compared to individual MJ1 clones in An. sinensis at the nucleotide level, high sequence identities were observed, ranging from 97% to nearly 99%. Similar high identities were also observed at the amino acid level. For example, the Aae_MJ1 in CONTIG_13910, the only Ae. aegypti MJ1 copy that has an intact open reading frame, shares 97% amino acid identity with Asi_MJ1_Clone1. The fact that full-length MJ1 elements from Aedes and Anopheles mosquitoes are highly similar at both nucleotide and the amino acid levels indicates the possibility of horizontal transfer, considering that the two genera had diverged 145–200 million years ago [16]. In comparison, the range of amino acid identities between randomly selected orthologous gene products in Ae. aegypti and An. gambiae was from 28 to 96% with an average of 43% [18].

Bottom Line: Among 24 mosquito species surveyed, MJ1 is only found in Ae. aegypti and the hyrcanus group of anopheline mosquitoes to which An. sinensis belongs.Therefore we have shown that it is feasible to use low coverage sequencing to systematically uncover horizontal transfer events.Expanding such efforts across a wide range of species will generate novel insights into the relative frequency of horizontal transfer of different TEs and provide the evolutionary context of these lateral transfer events.

View Article: PubMed Central - PubMed

Affiliation: Institute of Plant Physiology and Ecology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, Shanghai, China.

ABSTRACT
Horizontal transfer of genetic material between complex organisms often involves transposable elements (TEs). For example, a DNA transposon mariner has been shown to undergo horizontal transfer between different orders of insects and between different phyla of animals. Here we report the discovery and characterization of an ITmD37D transposon, MJ1, in Anopheles sinensis. We show that some MJ1 elements in Aedes aegypti and An. sinensis contain intact open reading frames and share nearly 99% nucleotide identity over the entire transposon, which is unexpectedly high given that these two genera had diverged 145-200 million years ago. Chromosomal hybridization and TE-display showed that MJ1 copy number is low in An. sinensis. Among 24 mosquito species surveyed, MJ1 is only found in Ae. aegypti and the hyrcanus group of anopheline mosquitoes to which An. sinensis belongs. Phylogenetic analysis is consistent with horizontal transfer and provides the basis for inference of its timing and direction. Although report of horizontal transfer of DNA transposons between higher eukaryotes is accumulating, our analysis is one of a small number of cases in which horizontal transfer of nearly identical TEs among highly divergent species has been thoroughly investigated and strongly supported. Horizontal transfer involving mosquitoes is of particular interest because there are ongoing investigations of the possibility of spreading pathogen-resistant genes into mosquito populations to control malaria and other infectious diseases. The initial indication of horizontal transfer of MJ1 came from comparisons between a 0.4x coverage An. sinensis 454 sequence database and available TEs in mosquito genomes. Therefore we have shown that it is feasible to use low coverage sequencing to systematically uncover horizontal transfer events. Expanding such efforts across a wide range of species will generate novel insights into the relative frequency of horizontal transfer of different TEs and provide the evolutionary context of these lateral transfer events.

Show MeSH
Related in: MedlinePlus