ena-STUDY-Genoscope CEA-11-12-2020-13:57:10:275-178
Massive colonization of protein-coding exons by selfish genetic elements in the germline genome of Paramecium aurelia species.
The presence of introns in eukaryotic genes has long remained a mystery for molecular biologists: why genes in pieces? A similar oddity exists in the germline genome of paramecia. Like [UdMO1] other ciliates, Paramecium is a unicellular eukaryote with both a germline genome (micronucleus, MIC), and a somatic genome (macronucleus, MAC) in the same cytoplasm. The MAC, responsible for gene expression, is not sexually transmitted but develops from a copy of the 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), that have to be precisely excised during the development of the new MAC to restore functional genes. To reconstruct the evolutionary history of this peculiar genomic architecture, we sequenced the MIC genomes of nine Paramecium species (from ~100 Mb in P. aurelia species to > 1.5 Gb in P. caudatum). We detected several waves of IES gains, notably at the basis of the P. aurelia clade and in the P. sonneborni lineage. Remarkably, we identified 24 families of mobile IESs that generated tens to thousands of new copies. The most active families show signature of horizontal transfer. These examples illustrate how DNA transposons can account for the massive proliferation of IESs in the germline genomes of Paramecium, both in non-coding regions and within exons. We also provide evidence that these elements represent a substantial burden for their host, presumably because of excision errors. Interestingly, we observe that IES excision pathways vary according to the age of IESs, and that older IESs tend to be more efficiently excised. This suggests that once fixed in the genome, the presence of IESs imposes a selective pressure on their host, both in cis (on the excision signals of each IES) and in trans (on the complex cellular machinery that triggers excision), to ensure efficient removal. Finally, we identified 69 IESs that are under strong purifying selection across the P. aurelia clade, which indicates that a small fraction of IESs have been domesticated during evolution to play a function beneficial for their host. All these features are highly reminiscent of the evolution of introns and illustrate the major impact of selfish elements, both on genome architecture and on the biology of the cell.
The presence of introns in eukaryotic genes has long remained a mystery for molecular biologists: why genes in pieces? A similar oddity exists in the germline genome of paramecia. Like [UdMO1] other ciliates, Paramecium is a unicellular eukaryote with both a germline genome (micronucleus, MIC), and a somatic genome (macronucleus, MAC) in the same cytoplasm. The MAC, responsible for gene expression, is not sexually transmitted but develops from a copy of the 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), that have to be precisely excised during the development of the new MAC to restore functional genes. To reconstruct the evolutionary history of this peculiar genomic architecture, we sequenced the MIC genomes of nine Paramecium species (from ~100 Mb in P. aurelia species to > 1.5 Gb in P. caudatum). We detected several waves of IES gains, notably at the basis of the P. aurelia clade and in the P. sonneborni lineage. Remarkably, we identified 24 families of mobile IESs that generated tens to thousands of new copies. The most active families show signature of horizontal transfer. These examples illustrate how DNA transposons can account for the massive proliferation of IESs in the germline genomes of Paramecium, both in non-coding regions and within exons. We also provide evidence that these elements represent a substantial burden for their host, presumably because of excision errors. Interestingly, we observe that IES excision pathways vary according to the age of IESs, and that older IESs tend to be more efficiently excised. This suggests that once fixed in the genome, the presence of IESs imposes a selective pressure on their host, both in cis (on the excision signals of each IES) and in trans (on the complex cellular machinery that triggers excision), to ensure efficient removal. Finally, we identified 69 IESs that are under strong purifying selection across the P. aurelia clade, which indicates that a small fraction of IESs have been domesticated during evolution to play a function beneficial for their host. All these features are highly reminiscent of the evolution of introns and illustrate the major impact of selfish elements, both on genome architecture and on the biology of the cell.