Limits...
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.

Show MeSH

Related in: MedlinePlus

Distribution of MJ1 in representatives of the mosquito species surveyed.Details and a full species list are provided in Table 1. The three species (Anopheles sinensis, Anopheles hyrcanus, and Aedes aegypti) that have MJ1 are highlighted by the horizontal lines. All other species do not have MJ1. The Anopheles and Aedes genera were estimated to have diverged 145–200 million years ago [16].
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3037385&req=5

pone-0016743-g004: Distribution of MJ1 in representatives of the mosquito species surveyed.Details and a full species list are provided in Table 1. The three species (Anopheles sinensis, Anopheles hyrcanus, and Aedes aegypti) that have MJ1 are highlighted by the horizontal lines. All other species do not have MJ1. The Anopheles and Aedes genera were estimated to have diverged 145–200 million years ago [16].

Mentions: A broad survey of MJ1 in 24 species within 5 genera is shown in Table 1. Presence or absence of MJ1 was determined by genomic PCR followed by sequencing. In the case of An. gambiae, An. stephensi, and Cx. quinquefasciatus, the absence of MJ1 was also confirmed by analysis of the genome assembly as well as trace files. MJ1 is restricted to Ae. aegypti and the hyrcanus group of Anopheles mosquitoes, to which An. sinensis belongs. As shown in Table 1, 10 of the 11 species within the hyrcanus group have MJ1 sequences. MJ1 was not found in eight Anopheles species outside the hyrcanus group, including An. lindesayi, a species that belongs to the same subgenus as the hyrcanus group. MJ1 was also not detected in four Culicinae mosquitoes, including Ae. albopictus, a species that is within the same subgenus as Ae. aegypti. All MJ1 copies that were obtained by PCR were confirmed by sequencing and special attention was paid to minimize false positive and false negative results as described in Methods and in Table 1. All MJ1 sequences, the nine genomic copies from Ae. aegypti and the 55 PCR clones from different Anopheles species within the hyrcanus group, are shown in Supplemental Files S1 and S2, respectively. An abbreviated schematic summary of the survey results is also shown in Figure 4, highlighting the fact that MJ1 is restricted to Ae. aegypti and the hyrcanus group of Anopheles mosquitoes. Overall, the pattern of patchy species distribution described in this section coupled with up to 99% sequence identity between MJ1 elements in Aedes and Anopheles mosquito species strongly suggests a recent horizontal transfer event.


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)

Distribution of MJ1 in representatives of the mosquito species surveyed.Details and a full species list are provided in Table 1. The three species (Anopheles sinensis, Anopheles hyrcanus, and Aedes aegypti) that have MJ1 are highlighted by the horizontal lines. All other species do not have MJ1. The Anopheles and Aedes genera were estimated to have diverged 145–200 million years ago [16].
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3037385&req=5

pone-0016743-g004: Distribution of MJ1 in representatives of the mosquito species surveyed.Details and a full species list are provided in Table 1. The three species (Anopheles sinensis, Anopheles hyrcanus, and Aedes aegypti) that have MJ1 are highlighted by the horizontal lines. All other species do not have MJ1. The Anopheles and Aedes genera were estimated to have diverged 145–200 million years ago [16].
Mentions: A broad survey of MJ1 in 24 species within 5 genera is shown in Table 1. Presence or absence of MJ1 was determined by genomic PCR followed by sequencing. In the case of An. gambiae, An. stephensi, and Cx. quinquefasciatus, the absence of MJ1 was also confirmed by analysis of the genome assembly as well as trace files. MJ1 is restricted to Ae. aegypti and the hyrcanus group of Anopheles mosquitoes, to which An. sinensis belongs. As shown in Table 1, 10 of the 11 species within the hyrcanus group have MJ1 sequences. MJ1 was not found in eight Anopheles species outside the hyrcanus group, including An. lindesayi, a species that belongs to the same subgenus as the hyrcanus group. MJ1 was also not detected in four Culicinae mosquitoes, including Ae. albopictus, a species that is within the same subgenus as Ae. aegypti. All MJ1 copies that were obtained by PCR were confirmed by sequencing and special attention was paid to minimize false positive and false negative results as described in Methods and in Table 1. All MJ1 sequences, the nine genomic copies from Ae. aegypti and the 55 PCR clones from different Anopheles species within the hyrcanus group, are shown in Supplemental Files S1 and S2, respectively. An abbreviated schematic summary of the survey results is also shown in Figure 4, highlighting the fact that MJ1 is restricted to Ae. aegypti and the hyrcanus group of Anopheles mosquitoes. Overall, the pattern of patchy species distribution described in this section coupled with up to 99% sequence identity between MJ1 elements in Aedes and Anopheles mosquito species strongly suggests a recent horizontal transfer event.

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