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

Osmanski, Austin; Paulat, Nicole S.; Korstian, Jennifer M.; Grimshaw, Jenna; Halsey, Michaela K.; Sullivan, Kevin A.; Moreno-Santillán, Diana D.; Crookshanks, Claudia; Roberts, Jacquelyn; Garcia, Carlos J.; Johnson, Matthew G.; Densmore, Llewellyn D.; Stevens, Richard D.; Rosen, Jeb; Storer, Jessica M.; Hubley, Robert; Smit, Arian F. A.; Dávalos, Liliana M.; Lindblad‐Toh, Kerstin; Karlsson, Elinor K.; Ray, David A.

doi:10.1101/2022.12.28.522108

Cited by 16 publications

(24 citation statements)

References 66 publications

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“…Compared to typical mammals, the newly sequenced bat genomes exhibited an accumulation of recent DNA transposon insertions (Supplementary Figure 5), similar to observations for other bats 42 .…”

Section: Ten New Reference-quality Chromosome-level Genomes Of Batssupporting

confidence: 76%

Reference-quality bat genomes illuminate adaptations to viral tolerance and disease resistance

Hiller

Morales

Ahmed

et al. 2023

Preprint

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Bats carry viruses that can cause severe disease in other mammals. Asymptomatic infections in bats suggest limited tissue-damaging inflammation and immunopathology. To investigate the genomic basis of disease resistance, the Bat1K project generated reference-quality genomes of ten bat species. A systematic analysis showed that signatures of selection in immune genes are more prevalent in bats compared with other mammals. We found an excess of immune gene adaptations in the ancestral Chiroptera and many descending bat lineages, highlighting viral entry and detection factors, and regulators of antiviral and inflammatory responses. ISG15, an antiviral gene contributing to hyperinflammation during COVID-19, exhibits a deletion of a cysteine, required for homodimer formation, in rhinolophid and hipposiderid bats. Cellular infection experiments showed enhanced intracellular protein conjugation of bat ISG15 and lack of secretion into extracellular space, where human ISG15 stimulates inflammation. Our work highlights molecular mechanisms contributing to viral tolerance and disease resistance in bats.

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Section: Ten New Reference-quality Chromosome-level Genomes Of Batssupporting

confidence: 76%

Reference-quality bat genomes illuminate adaptations to viral tolerance and disease resistance

Hiller

Morales

Ahmed

et al. 2023

Preprint

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“…At present, the lack of genome assemblies for sigmodontine rodents makes it challenging to study TEs in these species. However, a recent study examining TE content in mammals notes that cricetid rodents exhibit the highest rates of recent LTR retrotransposon accumulation among mammals ( Osmanski et al 2022 ). Overall, we hypothesize that for an ERV invasion to have a similar effect on LINE activity in another mammal, the causal ERV must arise from a divergent retrovirus (unfamiliar to host suppression machinery), show similar integration preference to that of LINEs, and rapidly evolve nonautonomous derivatives.…”

Section: Resultsmentioning

confidence: 99%

Transposable Element Interactions Shape the Ecology of the Deer Mouse Genome

Gozashti

Feschotte

Hoekstra

2023

Molecular Biology and Evolution

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The genomic landscape of transposable elements (TEs) varies dramatically across species, with some TEs demonstrating greater success in colonizing particular lineages than others. In mammals, LINE retrotransposons are typically more common than any other TE. Here, we report an unusual genomic landscape of TEs in the deer mouse, Peromyscus maniculatus. In contrast to other previously examined mammals, LTR elements occupy more of the deer mouse genome than LINEs (11% and 10% respectively). This pattern reflects a combination of relatively low LINE activity and a massive invasion of lineage-specific endogenous retroviruses (ERVs). Deer mouse ERVs exhibit diverse origins spanning the retroviral phylogeny suggesting they have been host to a wide range of exogenous retroviruses. Notably, we trace the origin of one ERV lineage, which arose ∼5-18 million years ago, to a close relative of feline leukemia virus, revealing inter-ordinal horizontal transmission. Several lineage-specific ERV subfamilies have very high copy numbers, with the top five most abundant accounting for ∼2% of the genome. We also observe a massive amplification of Kruppel-associated box domain-containing zinc finger genes (KZNFs), which likely control ERV activity and whose expansion may have been facilitated by ectopic recombination between ERVs. Finally, we find evidence that ERVs directly impacted the evolutionary trajectory of LINEs by outcompeting them for genomic sites and frequently disrupting autonomous LINE copies. Together, our results illuminate the genomic ecology that shaped the unique deer mouse TE landscape, shedding light on the evolutionary processes that give rise to variation in mammalian genome structure.

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Section: Resultsmentioning

confidence: 99%

“…We used a curated de novo TE library to annotate TE insertions in 250 eutherian mammalian species, including 37 bat species (Table S1) (Osmanski, et al 2022; Christmas, et al forthcoming). A general comparison of TE content among mammal assemblies is available elsewhere (Osmanski, et al 2022). Rather than recapitulate that work in illustrating general distinctions between bats and non-bats, we chose eight representative eutherians as our outgroup taxa.…”

Section: Resultsmentioning

confidence: 99%

“…We used the curated de novo transposable element (TE) consensus sequence library described in Osmanski et al (2022) to annotate TE insertions in all selected species using RepeatMasker v4.1.2-p1 (Smit, et al 2013(Smit, et al -2015 with the RMBlast search engine. Output was processed using RM2Bed.py, a utility in the RepeatMasker package, with TE insertion overlap resolution by lower divergence values (-o lower_div).…”

Section: Annotation Of Mammalian Transposable Element Insertionsmentioning

confidence: 99%

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

Paulat

Storer

Moreno-Santillán

et al. 2023

Preprint

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Horizontal transfer of transposable elements is an important mechanism contributing to genetic diversity and innovation. Bats (order Chiroptera) have repeatedly been shown to experience horizontal transfer of transposable elements at what appears to be a high rate compared to other mammals. We investigated the occurrence of horizontally transferred DNA transposons involving bats. We found over 200 putative horizontally transferred elements within bats; sixteen transposons were shared across distantly related mammalian clades and two 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.

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

Cited by 16 publications

References 66 publications

Reference-quality bat genomes illuminate adaptations to viral tolerance and disease resistance

Reference-quality bat genomes illuminate adaptations to viral tolerance and disease resistance

Transposable Element Interactions Shape the Ecology of the Deer Mouse Genome

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

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