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Genomes of historical specimens reveal multiple invasions of LTR retrotransposons in Drosophila melanogaster during the 19th century.

ABSTRACT: Transposable element invasions have a profound impact on the evolution of genomes and phenotypes. It is thus an important open question how often such TE invasions occur. To address this question, we utilize the genomes of historical specimens, sampled about 200 y ago. We found that the LTR retrotransposons Blood, Opus, and 412 spread in Drosophila melanogaster in the 19th century. These invasions constitute second waves, as degraded fragments were found for all three TEs. The composition of Opus and 412, but not of Blood, shows a pronounced geographic heterogeneity, likely due to founder effects during the invasions. Finally, we identified species from the Drosophila simulans complex as the likely origin of the TEs. We show that in total, seven TE families invaded D. melanogaster during the last 200y, thereby increasing the genome size by up to 1.2Mbp. We suggest that this high rate of TE invasions was likely triggered by human activity. Based on the analysis of strains and specimens sampled at different times, we provide a detailed timeline of TE invasions, making D. melanogaster the first organism where the invasion history of TEs during the last two centuries could be inferred.

SUBMITTER: Scarpa A

PROVIDER: S-EPMC11009621 | biostudies-literature | 2024 Apr

REPOSITORIES: biostudies-literature

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Genomes of historical specimens reveal multiple invasions of LTR retrotransposons in <i>Drosophila melanogaster</i> during the 19th century.

Scarpa Almorò A Pianezza Riccardo R Wierzbicki Filip F Kofler Robert R

Proceedings of the National Academy of Sciences of the United States of America 20240402 15

Transposable element invasions have a profound impact on the evolution of genomes and phenotypes. It is thus an important open question how often such TE invasions occur. To address this question, we utilize the genomes of historical specimens, sampled about 200 y ago. We found that the LTR retrotransposons Blood, Opus, and 412 spread in <i>Drosophila melanogaster</i> in the 19th century. These invasions constitute second waves, as degraded fragments were found for all three TEs. The composition ...[more]

PMID: 38564639

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Project description:BackgroundThe three superfamilies of Long Terminal Repeat (LTR) retrotransposons are a widespread kind of transposable element and a major factor in eukaryotic genome evolution. In metazoans, recent studies suggested that Copia LTR-retrotransposons display specific dynamic compared to the more abundant and diverse Gypsy elements. Indeed, Copia elements show a relative scarcity and the prevalence of only a few clades in specific hosts. Thus, BEL/Pao seems to be the second most abundant superfamily. However, the generality of these assumptions remains to be assessed. Therefore, we carried out the first large-scale comparative genomic analysis of LTR-retrotransposons in molluscs. The aim of this study was to analyse the diversity, copy numbers, genomic proportions and distribution of LTR-retrotransposons in a large host phylum.ResultsWe compare nine genomes of molluscs and further added LTR-retrotransposons sequences detected in databases for 47 additional species. We identified 1709 families, which enabled us to define 31 clades. We show that clade richness was highly dependent on the considered superfamily. We found only three Copia clades, including GalEa and Hydra which appear to be widely distributed and highly dominant as they account for 96% of the characterised Copia elements. Among the seven BEL/Pao clades identified, Sparrow and Surcouf are characterised for the first time. We find no BEL or Pao elements, but the rare clades Dan and Flow are present in molluscs. Finally, we characterised 21 Gypsy clades, only five of which had been previously described, the C-clade being the most abundant one. Even if they are found in the same number of host species, Copia elements are clearly less abundant than BEL/Pao elements in copy number or genomic proportions, while Gypsy elements are always the most abundant ones whatever the parameter considered.ConclusionsOur analysis confirms the contrasting dynamics of Copia and Gypsy elements in metazoans and indicates that BEL/Pao represents the second most abundant superfamily, probably reflecting an intermediate dynamic. Altogether, the data obtained in several taxa highly suggest that these patterns can be generalised for most metazoans. Finally, we highlight the importance of using database information in complement of genome analyses when analyzing transposable element diversity.

Project description:BackgroundLTR retrotransposons are a class of mobile genetic elements containing two similar long terminal repeats (LTRs). Currently, LTR retrotransposons are annotated in eukaryotic genomes mainly through the conventional homology searching approach. Hence, it is limited to annotating known elements.ResultsIn this paper, we report a de novo computational method that can identify new LTR retrotransposons without relying on a library of known elements. Specifically, our method identifies intact LTR retrotransposons by using an approximate string matching technique and protein domain analysis. In addition, it identifies partially deleted or solo LTRs using profile Hidden Markov Models (pHMMs). As a result, this method can de novo identify all types of LTR retrotransposons. We tested this method on the two pairs of eukaryotic genomes, C. elegans vs. C. briggsae and D. melanogaster vs. D. pseudoobscura. LTR retrotransposons in C. elegans and D. melanogaster have been intensively studied using conventional annotation methods. Comparing with previous work, we identified new intact LTR retroelements and new putative families, which may imply that there may still be new retroelements that are left to be discovered even in well-studied organisms. To assess the sensitivity and accuracy of our method, we compared our results with a previously published method, LTR_STRUC, which predominantly identifies full-length LTR retrotransposons. In summary, both methods identified comparable number of intact LTR retroelements. But our method can identify nearly all known elements in C. elegans, while LTR_STRUCT missed about 1/3 of them. Our method also identified more known LTR retroelements than LTR_STRUCT in the D. melanogaster genome. We also identified some LTR retroelements in the other two genomes, C. briggsae and D. pseudoobscura, which have not been completely finished. In contrast, the conventional method failed to identify those elements. Finally, the phylogenetic and chromosomal distributions of the identified elements are discussed.ConclusionWe report a novel method for de novo identification of LTR retrotransposons in eukaryotic genomes with favorable performance over the existing methods.

Dataset Information

Genomes of historical specimens reveal multiple invasions of LTR retrotransposons in Drosophila melanogaster during the 19th century.

Publications

Genomes of historical specimens reveal multiple invasions of LTR retrotransposons in <i>Drosophila melanogaster</i> during the 19th century.

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