Abstract

Transposable elements (TEs) are one of the major driving forces of genome evolution, raising the question of the long-term dynamics underlying their evolutionary success. Some TEs were proposed to evolve under a pattern of periodic extinctions-recolonizations, in which elements recurrently invade and quickly proliferate within their host genomes, then start to disappear until total extinction. Depending on the model, TE extinction is assumed to be driven by purifying selection against colonized host genomes (Sel-DE model) or by saturation of host genomes (Sat-DE model). Bacterial group II introns are suspected to follow an extinction-recolonization model of evolution, but whether they follow Sel-DE or Sat-DE dynamics is not known. Our analysis of almost 200 group II intron copies from 90 sequenced Enterobacteriales genomes confirms their extinction-recolonization dynamics: patchy element distributions among genera and even among strains within genera, acquisition of new group II introns through plasmids or other mobile genetic elements, and evidence for recent proliferations in some genomes. Distributions of recent and past proliferations and of their respective homing sites further provide strong support for the Sel-DE model, suggesting that group II introns are deleterious to their hosts. Overall, our observations emphasize the critical impact of host properties on TE dynamics.

Highlights

  • Transposable elements (TEs), which are mobilizing pieces of DNA, are widely distributed in eukaryote and prokaryote genomes, and they may represent substantial fractions of the genomes, as in Homo sapiens [1] or Zea Mays [2]

  • We searched for orthologous copies within genera/complexes to prevent counting several times copies that originated from a single ancestral insertion event, which would artificially inflate the overall abundance of group II introns in genera with more than one sequenced strain

  • Group II intron distribution in bacteria is known to be highly variable in abundance and diversity, suggesting periodic extinction-recolonization events [41,42,43]

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Summary

Introduction

Transposable elements (TEs), which are mobilizing pieces of DNA, are widely distributed in eukaryote and prokaryote genomes, and they may represent substantial fractions of the genomes, as in Homo sapiens [1] or Zea Mays [2]. TEs are major drivers of genome evolution, sometimes as actors of genetic innovation, or by creating genomic instability or genetic disorders [3,4,5] Given their relative deleteriousness, their tremendous evolutionary success results from a complex interplay between transposition rate, fitness cost, and host effective population size [6,7,8,9,10]. To explain the evolutionary success of IS elements in prokaryotes, a periodic extinction-recolonization model has been proposed, in which bacterial genomes undergo recurrent TE acquisitions and proliferations, followed by rapid elimination of the resulting TE copies [17] This scenario has recently received direct empirical evidence, based on the analysis of the unusual IS fossil record buried in the genomes of the bacterial endosymbiont Wolbachia [18]. TE acquisition is thought to be mainly achieved through larger mobile genetic elements (MGEs), especially plasmids which carry numerous IS elements [22]

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