Massive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Diamantis Sellis - , University of Lyon (Author)
  • Frédéric Guérin - , French National Centre for Scientific Research (CNRS) (Author)
  • Olivier Arnaiz - , French Alternative Energies and Atomic Energy Commission (CEA) (Author)
  • Walker Pett - , University of Lyon (Author)
  • Emmanuelle Lerat - , University of Lyon (Author)
  • Nicole Boggetto - , French National Centre for Scientific Research (CNRS) (Author)
  • Sascha Krenek - , Chair of Limnology (Author)
  • Thomas Berendonk - , Chair of Limnology (Author)
  • Arnaud Couloux - , Université d'Évry Val-d'Essonne (Author)
  • Jean Marc Aury - , Université d'Évry Val-d'Essonne (Author)
  • Karine Labadie - , Université Paris-Saclay (Author)
  • Sophie Malinsky - , French National Centre for Scientific Research (CNRS), Université Paris Cité (Author)
  • Simran Bhullar - , French National Centre for Scientific Research (CNRS) (Author)
  • Eric Meyer - , French National Centre for Scientific Research (CNRS) (Author)
  • Linda Sperling - , French Alternative Energies and Atomic Energy Commission (CEA) (Author)
  • Laurent Duret - , University of Lyon (Author)
  • Sandra Duharcourt - , French National Centre for Scientific Research (CNRS) (Author)

Abstract

a somatic genome in the same cytoplasm. The somatic macronucleus (MAC), responsible for gene expression, is not sexually transmitted but develops from a copy of the germline micronucleus (MIC) at each sexual generation. In the MIC genome of Paramecium tetraurelia, genes are interrupted by tens of thousands of unique intervening sequences called internal eliminated sequences (IESs), which have to be precisely excised during the development of the new MAC to restore functional genes. To understand the evolutionary origin of this peculiar genomic architecture, we sequenced the MIC genomes of 9 Paramecium species (from approximately 100 Mb in Paramecium aurelia species to >1.5 Gb in Paramecium caudatum). We detected several waves of IES gains, both in ancestral and in more recent lineages. While the vast majority of IESs are single copy in present-day genomes, we identified several families of mobile IESs, including nonautonomous elements acquired via horizontal transfer, which generated tens to thousands of new copies. These observations provide the first direct evidence that transposable elements can account for the massive proliferation of IESs in Paramecium. The comparison of IESs of different evolutionary ages indicates that, over time, IESs shorten and diverge rapidly in sequence while they acquire features that allow them to be more efficiently excised. We nevertheless identified rare cases of IESs that are under strong purifying selection across the aurelia clade. The cases examined contain or overlap cellular genes that are inactivated by excision during development, suggesting conserved regulatory mechanisms. Similar to the evolution of introns in eukaryotes, the evolution of Paramecium IESs highlights the major role played by selfish genetic elements in shaping the complexity of genome architecture and gene expression.

Details

Original languageEnglish
Article numbere3001309
JournalPLoS biology
Volume19
Issue number7
Publication statusPublished - Jul 2021
Peer-reviewedYes

External IDs

PubMed 34324490
ORCID /0000-0002-9301-1803/work/161409760