Insights into mammalian TE diversity through the curation of 248 genome assemblies

[INTRODUCTION] An estimated 160 million years have passed since the first placental mammals evolved. These eutherians are categorized into 19 orders consisting of nearly 4000 extant species, with ~70% being bats or rodents. Broad, in-depth, and comparative genomic studies across Eutheria have previously been unachievable because of the lack of genomic resources. The collaboration of the Zoonomia Consortium made available hundreds of high-quality genome assemblies for comparative analysis. Our focus within the consortium was to investigate the evolution of transposable elements (TEs) among placental mammals. Using these data, we identified previously known TEs, described previously unknown TEs, and analyzed the TE distribution among multiple taxonomic levels.[RATIONALE] The emergence of accurate and affordable sequencing technology has propelled efforts to sequence increasingly more nonmodel mammalian genomes in the past decade. Most of these efforts have traditionally focused on genic regions searching for patterns of selection or variation in gene regulation. The common trend of ignoring or trivializing TE annotation with newly published genomes has resulted in severe lag of TE analyses, leading to extensive undiscovered TE variation. This oversight has neglected an important source of evolution because the accumulation of TEs is attributable to drastic alterations in genome architecture, including insertions, deletions, duplications, translocations, and inversions. Our approach to the Zoonomia dataset was to provide future inquirers accurate and meticulous TE curations and to describe taxonomic variation among eutherians.[RESULTS] We annotated the TE content of 248 mammalian genome assemblies, which yielded a library of 25,676 consensus TE sequences, 8263 of which were previously unidentified TE sequences (available at https://dfam.org). We affirmed that the largest component of a typical mammalian genome is comprised of TEs (average 45.6%). Of the 248 assemblies, the lowest genomic percentage of TEs was found in the star-nosed mole (27.6%), and the largest percentage was seen in the aardvark (74.5%), whose increase in TE accumulation drove a corresponding increase in genome size—a correlation we observed across Eutheria. The overall genomic proportions of recently accumulated TEs were roughly similar across most mammals in the dataset, with a few notable exceptions (see the figure). Diversity of recently accumulated TEs is highest among multiple families of bats, mostly driven by substantial DNA transposon activity. Our data also exhibit an increase of recently accumulated DNA transposons among carnivore lineages over their herbivorous counterparts, which suggests that diet may play a role in determining the genomic content of TEs.[CONCLUSION] The copious TE data provided in this work emanated from the largest comprehensive TE curation effort to date. Considering the wide-ranging effects that TEs impose on genomic architecture, these data are an important resource for future inquiries into mammalian genomics and evolution and suggest avenues for continued study of these important yet understudied genomic denizens.This project was partially supported by NSF grant DEB 1838283 (D.D.M.-S. and D.A.R.), NSF grant IOS 2032006 (D.D.M.-S. and D.A.R.), National Institutes of Health (NIH) grant R01HG002939 (J.M.S., R.H., A.F.A.S., and J.Ros.), NIH grant U24HG010136 (J.M.S., R.H., A.F.A.S., and J.Ros.), NSF grant DEB 1838273 (L.M.D.), NSF grant DGE 1633299 (L.M.D.), NIH grant NHGRI R01HG008742 (Zoonomia Consortium), and a Swedish Research Council Distinguished Professor Award (Zoonomia Consortium).Peer reviewe

Insights into mammalian TE diversity through the curation of 248 genome assemblies.

We examined transposable element (TE) content of 248 placental mammal genome assemblies, the largest de novo TE curation effort in eukaryotes to date. We found that although mammals resemble one another in total TE content and diversity, they show substantial differences with regard to recent TE accumulation. This includes multiple recent expansion and quiescence events across the mammalian tree. Young TEs, particularly long interspersed elements, drive increases in genome size, whereas DNA transposons are associated with smaller genomes. Mammals tend to accumulate only a few types of TEs at any given time, with one TE type dominating. We also found association between dietary habit and the presence of DNA transposon invasions. These detailed annotations will serve as a benchmark for future comparative TE analyses among placental mammals

Insights into mammalian TE diversity through the curation of 248 genome assemblies.

We examined transposable element (TE) content of 248 placental mammal genome assemblies, the largest de novo TE curation effort in eukaryotes to date. We found that although mammals resemble one another in total TE content and diversity, they show substantial differences with regard to recent TE accumulation. This includes multiple recent expansion and quiescence events across the mammalian tree. Young TEs, particularly long interspersed elements, drive increases in genome size, whereas DNA transposons are associated with smaller genomes. Mammals tend to accumulate only a few types of TEs at any given time, with one TE type dominating. We also found association between dietary habit and the presence of DNA transposon invasions. These detailed annotations will serve as a benchmark for future comparative TE analyses among placental mammals

Chiropterans Are a Hotspot for Horizontal Transfer of DNA Transposons in Mammalia.

Horizontal transfer of transposable elements (TEs) is an important mechanism contributing to genetic diversity and innovation. Bats (order Chiroptera) have repeatedly been shown to experience horizontal transfer of TEs at what appears to be a high rate compared with other mammals. We investigated the occurrence of horizontally transferred (HT) DNA transposons involving bats. We found over 200 putative HT elements within bats; 16 transposons were shared across distantly related mammalian clades, and 2 other elements were shared with a fish and two lizard species. Our results indicate that bats are a hotspot for horizontal transfer of DNA transposons. These events broadly coincide with the diversification of several bat clades, supporting the hypothesis that DNA transposon invasions have contributed to genetic diversification of bats

Chiropterans are a hotspot for horizontal transfer of DNA transposons in mammalia

Horizontal transfer of transposable elements (TEs) is an important mechanism contributing to genetic diversity and innovation. Bats (order Chiroptera) have repeatedly been shown to experience horizontal transfer of TEs at what appears to be a high rate compared with other mammals. We investigated the occurrence of horizontally transferred (HT) DNA transposons involving bats. We found over 200 putative HT elements within bats; 16 transposons were shared across distantly related mammalian clades, and 2 other elements were shared with a fish and two lizard species. Our results indicate that bats are a hotspot for horizontal transfer of DNA transposons. These events broadly coincide with the diversification of several bat clades, supporting the hypothesis that DNA transposon invasions have contributed to genetic diversification of bats

Chiropterans are a hotspot for horizontal transfer of DNA transposons in mammalia

This project was supported by the National Science Foundation (grant numbers DEB 1838283 and IOS 2032006 to D.M.-S. and Dav.R. and DEB 1838273 and DGE 1633299 to L.D.), National Institutes of Health (grant numbers R01HG002939 and U24HG010136 to J.S., R.H., A.F.A.S., and Je.R.), NHGRI (grant number R01HG008742 to Z.C.), Irish Research Council (grant number IRCLA/ 2017/58 to E.T.), Science Foundation Ireland (grant number 19/FFP/6790 to E.T.), Max Planck Research Group awarded by the Max Planck Gesellschaft to S.V., Human Frontiers Science Program (grant number RGP0058/2016 to S.V.), UK Research and Innovation (grant number MR/T021985/1 to S.V.), and the Swedish Research Council Distinguished Professor Award to K.L.-T.Horizontal transfer of transposable elements (TEs) is an important mechanism contributing to genetic diversity and innovation. Bats (order Chiroptera) have repeatedly been shown to experience horizontal transfer of TEs at what appears to be a high rate compared with other mammals. We investigated the occurrence of horizontally transferred (HT) DNA transposons involving bats. We found over 200 putative HT elements within bats; 16 transposons were shared across distantly related mammalian clades, and 2 other elements were shared with a fish and two lizard species. Our results indicate that bats are a hotspot for horizontal transfer of DNA transposons. These events broadly coincide with the diversification of several bat clades, supporting the hypothesis that DNA transposon invasions have contributed to genetic diversification of bats.Publisher PDFPeer reviewe