Transposable elements are constantly exchanged by horizontal transfer reshaping mosquito genomes

Abstract

AbstractTransposable elements (TEs) are a set of mobile elements within a genome. Due to their complexity, an in-depth TE characterization is only available for a handful of model organisms. In the present study, we performed ade novoand homology-based characterization of TEs in the genomes of 24 mosquito species and investigated their mode of inheritance. More than 40% of the genome ofAedes aegypti, Aedes albopictus, andCulex quinquefasciatusis composed of TEs, varying substantially amongAnophelesspecies (0.13%–19.55%). Class I TEs are the most abundant among mosquitoes and at least 24 TE superfamilies were found. Interestingly, TEs have been continuously exchanged by horizontal transfer (212 TE families of 18 different superfamilies) among mosquitoes since 30 million years ago, representing around 6% of the genome inAedesgenomes and a small fraction inAnophelesgenomes. Most of these horizontally transferred TEs are from the three ubiquitous LTR superfamilies: Gypsy, Bel-Pao and Copia. Searching more 32,000 genomes, we also uncover transfers between mosquitoes and two different Phyla—Cnidaria and Nematoda—and two subphyla—Chelicerata and Crustacea, identifying a vector, the wormWuchereria bancrofti, that enabled the horizontal spread of a Tc1-mariner element ofirritanssubfamily among variousAnophelesspecies. These data also allowed us to reconstruct the horizontal transfer network of this TE involving more than 40 species. In summary, our results suggest that TEs are constantly exchanged by common phenomena of horizontal transfers among mosquitoes, influencing genome variation and contributing to genome size expansion.Author SummaryMost eukaryotes have DNA fragments inside their genome that can multiply by inserting themselves in other regions of the genome, generating variability. These fragments are called Transposable Elements (TEs). Since they are a constituent part of the eukaryote genomes, these pieces of DNA are usually inherited vertically by the offspring. To avoid damage to the genome caused by the replication and insertion of TEs, organisms usually control them, leading to their inactivation. However, TEs sometimes get out of control and invade other species through a horizontal transfer mechanism. This dynamic is not known in mosquitoes, a group of organisms that acts as vectors of many human diseases. We collected mosquito genomes available in public databases and characterized the whole content of TEs. Using a statistic supported method, we investigate TE relations among mosquitoes and discover that horizontal transfers of transposons are common and occurred in the last 30 million years among these species. Although not as common as transfers among closely related species, transposon transfer to distant species also occur. We also identify a parasite, a filarial worm, that may have facilitated the transfer of TE to many mosquitoes. Together, horizontally transferred TEs contribute to increasing mosquito genome size and variation.