Horizontal Transfer Of Transposable Elements Research Articles

Multiple horizontal transfer events of a DNA transposon into turtles, fishes, and a frog

Horizontal transfer of transposable elements (HTT) has been reported across many species and the impact of such events on genome structure and function has been well described. However, few studies have focused on reptilian genomes, especially HTT events in Testudines (turtles). Here, as a consequence of investigating the repetitive content of Malaclemys terrapin terrapin (Diamondback turtle) we found a high similarity DNA transposon, annotated in RepBase as hAT-6_XT, shared between other turtle species, ray-finned fishes, and a frog. hAT-6_XT was notably absent in reptilian taxa closely related to turtles, such as crocodiles and birds. Successful invasion of DNA transposons into new genomes requires the conservation of specific residues in the encoded transposase, and through structural analysis, these residues were identified indicating some retention of functional transposition activity. We document six recent independent HTT events of a DNA transposon in turtles, which are known to have a low genomic evolutionary rate and ancient repeats.

Modeling early germline immunization after horizontal transfer of transposable elements reveals internal piRNA cluster heterogeneity

BackgroundA fraction of all genomes is composed of transposable elements (TEs) whose mobility needs to be carefully controlled. In gonads, TE activity is repressed by PIWI-interacting RNAs (piRNAs), a class of small RNAs synthesized by heterochromatic loci enriched in TE fragments, called piRNA clusters. Maintenance of active piRNA clusters across generations is secured by maternal piRNA inheritance providing the memory for TE repression. On rare occasions, genomes encounter horizontal transfer (HT) of new TEs with no piRNA targeting them, threatening the host genome integrity. Naïve genomes can eventually start to produce new piRNAs against these genomic invaders, but the timing of their emergence remains elusive.ResultsUsing a set of TE-derived transgenes inserted in different germline piRNA clusters and functional assays, we have modeled a TE HT in Drosophila melanogaster. We have found that the complete co-option of these transgenes by a germline piRNA cluster can occur within four generations associated with the production of new piRNAs all along the transgenes and the germline silencing of piRNA sensors. Synthesis of new transgenic TE piRNAs is linked to piRNA cluster transcription dependent on Moonshiner and heterochromatin mark deposition that propagates more efficiently on short sequences. Moreover, we found that sequences located within piRNA clusters can have different piRNA profiles and can influence transcript accumulation of nearby sequences.ConclusionsOur study reveals that genetic and epigenetic properties, such as transcription, piRNA profiles, heterochromatin, and conversion efficiency along piRNA clusters, could be heterogeneous depending on the sequences that compose them. These findings suggest that the capacity of transcriptional signal erasure induced by the chromatin complex specific of the piRNA cluster can be incomplete through the piRNA cluster loci. Finally, these results have revealed an unexpected level of complexity that highlights a new magnitude of piRNA cluster plasticity fundamental for the maintenance of genome integrity.

The P-element Has Not Significant Effect on the <i>Drosophila simulans</i> Viability

Cases of horizontal transfer of transposable elements (TEs) between species are known for the Drosophilidae family. In the middle of the last century, the case of horizontal transfer of the P-element from the Drosophila willistoni to the D. melanogaster was described. A novel P-element invasion into the D. simulans genome from D. melanogaster occurred approximately 10 years ago. Currently, the P-element has spread across all D. melanogaster population and 30% of D. simulans populations in Europe, Africa and America. In this paper, we investigated the presence of the P-element in D. simulans lines caught in different years in three Asian populations (Tashkent, Nalchik and Sakhalin Island). We also examined the physiological characteristics (cytotype, lifespan, fecundity and locomotor activity) of D. simulans lines with and without the P-element to determine the significance of this new mobile element in the genome. The P-element was found in lines isolated from nature after 2012. The number of P-element copies per genome (two-to-three dozen according to fluorescence in situ hybridization data) was greater than in the American and comparable to the African populations. There were signs of intraspecific hybrid dysgenesis for some pairs of lines. However, in general the presence of the P-element did not adversely affect the physiological characteristics. Either adaptation to the new TE occurs very quickly, or the rate of movement of the P-element is so insignificant that its appearance in the genome remains unnoticed.

The P-Element Has Not Significant Effect on the Drosophila simulans Viability

Cases of horizontal transfer of transposable elements (TEs) between species are known for the Drosophilidae family. In the middle of the last century, the case of horizontal transfer of the P-element from the Drosophila willistoni to the D. melanogaster was described. A novel P-element invasion into the D. simulans genome from D. melanogaster occurred approximately 10 years ago. Currently, the P-element has spread across all D. melanogaster population and 30% of D. simulans populations in Europe, Africa and America. In this paper, we investigated the presence of the P-element in D. simulans lines caught in different years in three Asian populations (Tashkent, Nalchik and Sakhalin Island). We also examined the physiological characteristics (cytotype, lifespan, fecundity and locomotor activity) of D. simulans lines with and without the P-element to determine the significance of this new mobile element in the genome. The P-element was found in lines isolated from nature after 2012. The number of P-element copies per genome (two-to-three dozen according to fluorescence in situ hybridization data) was greater than in the American and comparable to the African populations. There were signs of intraspecific hybrid dysgenesis for some pairs of lines. However, in general the presence of the P-element did not adversely affect the physiological characteristics. Either adaptation to the new TE occurs very quickly, or the rate of movement of the P-element is so insignificant that its appearance in the genome remains unnoticed.

Sample Sequence Analysis Uncovers Recurrent Horizontal Transfers of Transposable Elements among Grasses.

Limited genome resources are a bottleneck in the study of horizontal transfer (HT) of DNA in plants. To solve this issue, we tested the usefulness of low-depth sequencing data generated from 19 previously uncharacterized panicoid grasses for HT investigation. We initially searched for horizontally transferred LTR-retrotransposons by comparing the 19 sample sequences to 115 angiosperm genome sequences. Frequent HTs of LTR-retrotransposons were identified solely between panicoids and rice (Oryza sativa). We consequently focused on additional Oryza species and conducted a nontargeted investigation of HT involving the panicoid genus Echinochloa, which showed the most HTs in the first set of analyses. The comparison of nine Echinochloa samples and ten Oryza species identified recurrent HTs of diverse transposable element (TE) types at different points in Oryza history, but no confirmed cases of HT for sequences other than TEs. One case of HT was observed from one Echinochloa species into one Oryza species with overlapping geographic distributions. Variation among species and data sets highlights difficulties in identifying all HT, but our investigations showed that sample sequence analyses can reveal the importance of HT for the diversification of the TE repertoire of plants.

Horizontal transfer and evolution of transposable elements in vertebrates

Horizontal transfer of transposable elements (HTT) is an important process shaping eukaryote genomes, yet very few studies have quantified this phenomenon on a large scale or have evaluated the selective constraints acting on transposable elements (TEs) during vertical and horizontal transmission. Here we screen 307 vertebrate genomes and infer a minimum of 975 independent HTT events between lineages that diverged more than 120 million years ago. HTT distribution greatly differs from null expectations, with 93.7% of these transfers involving ray-finned fishes and less than 3% involving mammals and birds. HTT incurs purifying selection (conserved protein evolution) on all TEs, confirming that producing functional transposition proteins is required for a TE to invade new genomes. In the absence of HTT, DNA transposons appear to evolve neutrally within genomes, unlike most retrotransposons, which evolve under purifying selection. This selection regime indicates that proteins of most retrotransposon families tend to process their own encoding RNA (cis-preference), which helps retrotransposons to persist within host lineages over long time periods.

High frequency of horizontal transfer in Jockey families (LINE order) of drosophilids

BackgroundThe use of large-scale genomic analyses has resulted in an improvement of transposable element sampling and a significant increase in the number of reported HTT (horizontal transfer of transposable elements) events by expanding the sampling of transposable element sequences in general and of specific families of these elements in particular, which were previously poorly sampled. In this study, we investigated the occurrence of HTT events in a group of elements that, until recently, were uncommon among the HTT records in Drosophila – the Jockey elements, members of the LINE (long interspersed nuclear element) order of non-LTR (long terminal repeat) retrotransposons. The sequences of 111 Jockey families deposited in Repbase that met the criteria of the analysis were used to identify Jockey sequences in 48 genomes of Drosophilidae (genus Drosophila, subgenus Sophophora: melanogaster, obscura and willistoni groups; subgenus Drosophila: immigrans, melanica, repleta, robusta, virilis and grimshawi groups; subgenus Dorsilopha: busckii group; genus/subgenus Zaprionus and genus Scaptodrosophila).ResultsPhylogenetic analyses revealed 72 Jockey families in 41 genomes. Combined analyses revealed 15 potential HTT events between species belonging to different genera and species groups of Drosophilidae, providing evidence for the flow of genetic material favoured by the spatio-temporal sharing of these species present in the Palaeartic or Afrotropical region.ConclusionsOur results provide phylogenetic, biogeographic and temporal evidence of horizontal transfers of the Jockey elements, increase the number of rare records of HTT in specific families of LINE elements, increase the number of known occurrences of these events, and enable a broad understanding of the evolutionary dynamics of these elements and the host species.

Helena and BS: Two Travellers between the Genera Drosophila and Zaprionus.

The frequency of horizontal transfers of transposable elements (HTTs) varies among the types of elements according to the transposition mode and the geographical and temporal overlap of the species involved in the transfer. The drosophilid species of the genus Zaprionus and those of the melanogaster, obscura, repleta, and virilis groups of the genus Drosophila investigated in this study shared space and time at some point in their evolutionary history. This is particularly true of the subgenus Zaprionus and the melanogaster subgroup, which overlapped both geographically and temporally in Tropical Africa during their period of origin and diversification. Here, we tested the hypothesis that this overlap may have facilitated the transfer of retrotransposons without long terminal repeats (non-LTRs) between these species. We estimated the HTT frequency of the non-LTRs BS and Helena at the genome-wide scale by using a phylogenetic framework and a vertical and horizontal inheritance consistence analysis (VHICA). An excessively low synonymous divergence among distantly related species and incongruities between the transposable element and species phylogenies allowed us to propose at least four relatively recent HTT events of Helena and BS involving ancestors of the subgroup melanogaster and ancestors of the subgenus Zaprionus during their concomitant diversification in Tropical Africa, along with older possible events between species of the subgenera Drosophila and Sophophora. This study provides the first evidence for HTT of non-LTRs retrotransposons between Drosophila and Zaprionus, including an in-depth reconstruction of the time frame and geography of these events.

HTT-DB: new features and updates.

Horizontal Transfer (HT) of genetic material between species is a common phenomenon among Bacteria and Archaea species and several databases are available for information retrieval and data mining. However, little attention has been given to this phenomenon among eukaryotic species mainly due to the lower proportion of these events. In the last years, a vertiginous amount of new HT events involving eukaryotic species was reported in the literature, highlighting the need of a common repository to keep the scientific community up to date and describe overall trends. Recently, we published the first HT database focused on HT of transposable elements among eukaryotes: the Horizontal Transposon Transfer DataBase: Database URL: (http://lpa.saogabriel.unipampa.edu.br: 8080/httdatabase/). Here, we present new features and updates of this unique database: (i) its expansion to include virus-host exchange of genetic material, which we called Horizontal Virus Transfer (HVT) and (ii) the availability of a web server for HT detection, where we implemented the online version of vertical and horizontal inheritance consistence analysis (VHICA), an R package developed for HT detection. These improvements will help researchers to navigate through known HVT cases, take data-informed decision and export figures based on keywords searches. Moreover, the availability of the VHICA as an online tool will make this software easily reachable even for researchers with no or little computation knowledge as well as foster our capability to detect new HT events in a wide variety of taxa. Database URL: http://lpa.saogabriel.unipampa.edu.br:8080/httdatabase/

Analyzing Horizontal Transfer of Transposable Elements on a Large Scale: Challenges and Prospects.

Whoever compares the genomes of distantly related species might find aberrantly high sequence similarity at certain loci. Such anomaly can only be explained by genetic material being transferred through other means than reproduction, that is, a horizontal transfer (HT). Between multicellular organisms, the transferred material will likely turn out to be a transposable element (TE). Because TEs can move between loci and invade chromosomes by replicating themselves, HT of TEs (HTT) profoundly impacts genome evolution. Yet, very few studies have quantified HTT at large taxonomic scales. Indeed, this task currently faces difficulties that range from the variable quality of available genome sequences to limitations of analytical procedures, some of which have been overlooked. Here we review the many challenges that an extensive analysis of HTT must overcome, we expose biases and limits of current methods, suggest solutions or workarounds, and reflect upon approaches that could be developed to better quantify this phenomenon.

Massive horizontal transfer of transposable elements in insects

Horizontal transfer (HT) of genetic material is central to the architecture and evolution of prokaryote genomes. Within eukaryotes, the majority of HTs reported so far are transfers of transposable elements (TEs). These reports essentially come from studies focusing on specific lineages or types of TEs. Because of the lack of large-scale survey, the amount and impact of HT of TEs (HTT) in eukaryote evolution, as well as the trends and factors shaping these transfers, are poorly known. Here, we report a comprehensive analysis of HTT in 195 insect genomes, representing 123 genera and 13 of the 28 insect orders. We found that these insects were involved in at least 2,248 HTT events that essentially occurred during the last 10 My. We show that DNA transposons transfer horizontally more often than retrotransposons, and unveil phylogenetic relatedness and geographical proximity as major factors facilitating HTT in insects. Even though our study is restricted to a small fraction of insect biodiversity and to a recent evolutionary timeframe, the TEs we found to be horizontally transferred generated up to 24% (2.08% on average) of all nucleotides of insect genomes. Together, our results establish HTT as a major force shaping insect genome evolution.

Ecological networks to unravel the routes to horizontal transposon transfers.

Transposable elements (TEs) represent the single largest component of numerous eukaryotic genomes, and their activity and dispersal constitute an important force fostering evolutionary innovation. The horizontal transfer of TEs (HTT) between eukaryotic species is a common and widespread phenomenon that has had a profound impact on TE dynamics and, consequently, on the evolutionary trajectory of many species' lineages. However, the mechanisms promoting HTT remain largely unknown. In this article, we argue that network theory combined with functional ecology provides a robust conceptual framework and tools to delineate how complex interactions between diverse organisms may act in synergy to promote HTTs.

Horizontal transfers of transposable elements in eukaryotes: The flying genes

Transposable elements (TEs) are the major components of eukaryotic genomes. Their propensity to densely populate and in some cases invade the genomes of plants and animals is in contradiction with the fact that transposition is strictly controlled by several molecular pathways acting at either transcriptional or post-transcriptional levels. Horizontal transfers, defined as the transmission of genetic material between sexually isolated species, have long been considered as rare phenomena. Here, we show that the horizontal transfers of transposable elements (HTTs) are very frequent in ecosystems. The exact mechanisms of such transfers are not well understood, but species involved in close biotic interactions, like parasitism, show a propensity to exchange genetic material horizontally. We propose that HTTs allow TEs to escape the silencing machinery of their host genome and may therefore be an important mechanism for their survival and their dissemination in eukaryotes.

Population genomics supports baculoviruses as vectors of horizontal transfer of insect transposons

Horizontal transfer (HT) of DNA is an important factor shaping eukaryote evolution. Although several hundreds of eukaryote-to-eukaryote HTs of transposable elements (TEs) have been reported, the vectors underlying these transfers remain elusive. Here, we show that multiple copies of two TEs from the cabbage looper (Trichoplusia ni) transposed in vivo into genomes of the baculovirus Autographa californica multiple nucleopolyhedrovirus (AcMNPV) during caterpillar infection. We further demonstrate that both TEs underwent recent HT between several sympatric moth species (T. ni, Manduca sexta, Helicoverpa spp.) showing different degrees of susceptibility to AcMNPV. Based on two independent population genomics data sets (reaching a total coverage >330,000X), we report a frequency of one moth TE in ~8,500 AcMNPV genomes. Together, our results provide strong support for the role of viruses as vectors of TE HT between animals, and they call for a systematic evaluation of the frequency and impact of virus-mediated HT on the evolution of host genomes.

Widespread and frequent horizontal transfers of transposable elements in plants

Vertical, transgenerational transmission of genetic material occurs through reproduction of living organisms. In addition to vertical inheritance, horizontal gene transfer between reproductively isolated species has recently been shown to be an important, if not dominant, mechanism in the evolution of prokaryotic genomes. In contrast, only a few horizontal transfer (HT) events have been characterized so far in eukaryotes and mainly concern transposable elements (TEs). Whether these are frequent and have a significant impact on genome evolution remains largely unknown. We performed a computational search for highly conserved LTR retrotransposons among 40 sequenced eukaryotic genomes representing the major plant families. We found that 26 genomes (65%) harbor at least one case of horizontal TE transfer (HTT). These transfers concern species as distantly related as palm and grapevine, tomato and bean, or poplar and peach. In total, we identified 32 cases of HTTs, which could translate into more than 2 million among the 13,551 monocot and dicot genera. Moreover, we show that these TEs have remained functional after their transfer, occasionally causing a transpositional burst. This suggests that plants can frequently exchange genetic material through horizontal transfers and that this mechanism may be important in TE-driven genome evolution.

Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution

In contrast to vertical gene transfer from parent to offspring, horizontal (or lateral) gene transfer moves genetic information between different species. Bacteria and archaea often adapt through horizontal gene transfer. Recent analyses indicate that eukaryotic genomes, too, have acquired numerous genes via horizontal transfer from prokaryotes and other lineages. Based on this we raise the hypothesis that horizontally acquired genes may have contributed more to adaptive evolution of eukaryotes than previously assumed. Current candidate sets of horizontally acquired eukaryotic genes may just be the tip of an iceberg. We have recently shown that adaptation of the thermoacidophilic red alga Galdieria sulphuraria to its hot, acid, toxic-metal laden, volcanic environment was facilitated by the acquisition of numerous genes from extremophile bacteria and archaea. Other recently published examples of horizontal acquisitions involved in adaptation include ice-binding proteins in marine algae, enzymes for carotenoid biosynthesis in aphids, and genes involved in fungal metabolism. Editor's suggested further reading in BioEssays Jumping the fine LINE between species: Horizontal transfer of transposable elements in animals catalyses genome evolutionAbstract.

Horizontal gene transfer in plants

Horizontal gene transfer (HGT) describes the transmission of genetic material across species boundaries. HGT often occurs in microbic and eukaryotic genomes. However, the pathways by which HGTs occur in multicellular eukaryotes, especially in plants, are not well understood. We systematically summarized more than ten possible pathways for HGT. The intimate contact which frequently occurs in parasitism, symbiosis, pathogen, epiphyte, entophyte, and grafting interactions could promote HGTs between two species. Besides these direct transfer methods, genes can be exchanged with a vector as a bridge: possible vectors include pollen, fungi, bacteria, viruses, viroids, plasmids, transposons, and insects. HGT, especially when involving horizontal transfer of transposable elements, is recognized as a significant force propelling genomic variation and biological innovation, playing an important functional and evolutionary role in both eukaryotic and prokaryotic genomes. We proposed possible mechanisms by which HGTs can occur, which is useful in understanding the genetic information exchange among distant species or distant cellular components.

Jumping the fine LINE between species: Horizontal transfer of transposable elements in animals catalyses genome evolution

Horizontal transfer (HT) is the transmission of genetic material between non-mating species, a phenomenon thought to occur rarely in multicellular eukaryotes. However, many transposable elements (TEs) are not only capable of HT, but have frequently jumped between widely divergent species. Here we review and integrate reported cases of HT in retrotransposons of the BovB family, and DNA transposons, over a broad range of animals spanning all continents. Our conclusions challenge the paradigm that HT in vertebrates is restricted to infective long terminal repeat (LTR) retrotransposons or retroviruses. This raises the possibility that other non-LTR retrotransposons, such as L1 or CR1 elements, believed to be only vertically transmitted, can horizontally transfer between species. Growing evidence indicates that the process of HT is much more general across different TEs and species than previously believed, and that it likely shapes eukaryotic genomes and catalyses genome evolution.

Horizontal transfer of OC1 transposons in the Tasmanian devil

BackgroundThere is growing recognition that horizontal DNA transfer, a process known to be common in prokaryotes, is also a significant source of genomic variation in eukaryotes. Horizontal transfer of transposable elements (HTT) may be especially prevalent in eukaryotes given the inherent mobility, widespread occurrence, and prolific abundance of these elements in many eukaryotic genomes.ResultsHere, we provide evidence for a new case of HTT of the transposon family OposCharlie1 (OC1) in the Tasmanian devil, Sarcophilus harrisii. Bioinformatic analyses of OC1 sequences in the Tasmanian devil genome suggest that this transposon infiltrated the common ancestor of the Dasyuridae family ~17 million years ago. This estimate is corroborated by a PCR-based screen for the presence/absence of this family in Tasmanian devils and closely-related species.ConclusionsThis case of HTT is the first to be reported in dasyurids. It brings the number of animal lineages independently invaded by OC1 to 12, and adds a fourth continent to the pandemic-like pattern of invasion of this transposon. In the context of these data, we discuss the evolutionary history of this transposon family and its potential impact on the diversification of marsupials.

Cargo capacity of phages and plasmids and other factors influencing horizontal transfers of prokaryote transposable elements

Horizontal transfer of transposable elements (TEs) plays a key role in prokaryote genome evolution. Most TEs do not encode the enzymatic machinery allowing them to transfer between host cells and it is widely assumed in the literature that horizontal transfer of prokaryote TEs is mediated by other mobile genetic elements such as phages and plasmids. In a recent study, we have shown that phages are less tolerant to insertion sequences (IS, the most frequent class of prokaryote TEs) and therefore have a lower cargo capacity than plasmids. Consequently, while our analysis confirmed the crucial role of plasmids as efficient vehicles of IS horizontal transfer, we concluded that phages are unlikely to efficiently shuttle IS elements between prokaryotes. Here, we discuss whether or not the distribution pattern observed for IS elements in phages and plasmids also holds for other TEs, such as transposons and mobile introns. We also further explore various factors that may impact the relative capacity of phages and plasmids to mediate TE horizontal transfer among prokaryotes.