Mosquito genomes are frequently invaded by transposable elements through horizontal transfer

PLoS Genet. 2020 Nov 30;16(11):e1008946. doi: 10.1371/journal.pgen.1008946. eCollection 2020 Nov.

Abstract

Transposable elements (TEs) are mobile genetic elements that parasitize basically all eukaryotic species genomes. Due to their complexity, an in-depth TE characterization is only available for a handful of model organisms. In the present study, we performed a de novo and homology-based characterization of TEs in the genomes of 24 mosquito species and investigated their mode of inheritance. More than 40% of the genome of Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus is composed of TEs, while it varied substantially among Anopheles species (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 extensively exchanged by horizontal transfer (172 TE families of 16 different superfamilies) among mosquitoes in the last 30 million years. Horizontally transferred TEs represents around 7% of the genome in Aedes species and a small fraction in Anopheles genomes. Most of these horizontally transferred TEs are from the three ubiquitous LTR superfamilies: Gypsy, Bel-Pao and Copia. Searching more than 32,000 genomes, we also uncovered transfers between mosquitoes and two different Phyla-Cnidaria and Nematoda-and two subphyla-Chelicerata and Crustacea, identifying a vector, the worm Wuchereria bancrofti, that enabled the horizontal spread of a Tc1-mariner element among various Anopheles species. 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 frequently exchanged by horizontal transfers among mosquitoes, influencing mosquito's genome size and variability.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anopheles / genetics
  • Culicidae / genetics*
  • DNA Transposable Elements / genetics*
  • Databases, Genetic
  • Evolution, Molecular
  • Gene Transfer, Horizontal / genetics*
  • Genome / genetics
  • Mosquito Vectors / genetics
  • Phylogeny
  • Retroelements

Substances

  • DNA Transposable Elements
  • Retroelements

Associated data

  • figshare/10.6084/m9.figshare.11336207

Grants and funding

This project was supported by the National Council for Scientific and Technological Development by the productivity research fellowship level 2 for Wallau GL (303902/2019-1) and by Fundação Oswaldo Cruz and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) under the project numbers PROEP/IAM (406667/2016-0 and 400742/2019-5). Melo, ES received a PhD scholarship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.