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

Ciliates are unicellular eukaryotes with both a germline genome and 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 g...

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Autores principales:	Diamantis Sellis, Frédéric Guérin, Olivier Arnaiz, Walker Pett, Emmanuelle Lerat, Nicole Boggetto, Sascha Krenek, Thomas Berendonk, Arnaud Couloux, Jean-Marc Aury, Karine Labadie, Sophie Malinsky, Simran Bhullar, Eric Meyer, Linda Sperling, Laurent Duret, Sandra Duharcourt
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/8e5fba611f9b49129c2ba90f7930162b
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spelling	oai:doaj.org-article:8e5fba611f9b49129c2ba90f7930162b2021-12-02T19:54:21ZMassive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes.1544-91731545-788510.1371/journal.pbio.3001309https://doaj.org/article/8e5fba611f9b49129c2ba90f7930162b2021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pbio.3001309https://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Ciliates are unicellular eukaryotes with both a germline genome and 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.Diamantis SellisFrédéric GuérinOlivier ArnaizWalker PettEmmanuelle LeratNicole BoggettoSascha KrenekThomas BerendonkArnaud CoulouxJean-Marc AuryKarine LabadieSophie MalinskySimran BhullarEric MeyerLinda SperlingLaurent DuretSandra DuharcourtPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 19, Iss 7, p e3001309 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Diamantis Sellis Frédéric Guérin Olivier Arnaiz Walker Pett Emmanuelle Lerat Nicole Boggetto Sascha Krenek Thomas Berendonk Arnaud Couloux Jean-Marc Aury Karine Labadie Sophie Malinsky Simran Bhullar Eric Meyer Linda Sperling Laurent Duret Sandra Duharcourt Massive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes.
description	Ciliates are unicellular eukaryotes with both a germline genome and 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.
format	article
author	Diamantis Sellis Frédéric Guérin Olivier Arnaiz Walker Pett Emmanuelle Lerat Nicole Boggetto Sascha Krenek Thomas Berendonk Arnaud Couloux Jean-Marc Aury Karine Labadie Sophie Malinsky Simran Bhullar Eric Meyer Linda Sperling Laurent Duret Sandra Duharcourt
author_facet	Diamantis Sellis Frédéric Guérin Olivier Arnaiz Walker Pett Emmanuelle Lerat Nicole Boggetto Sascha Krenek Thomas Berendonk Arnaud Couloux Jean-Marc Aury Karine Labadie Sophie Malinsky Simran Bhullar Eric Meyer Linda Sperling Laurent Duret Sandra Duharcourt
author_sort	Diamantis Sellis
title	Massive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes.
title_short	Massive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes.
title_full	Massive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes.
title_fullStr	Massive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes.
title_full_unstemmed	Massive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes.
title_sort	massive colonization of protein-coding exons by selfish genetic elements in paramecium germline genomes.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/8e5fba611f9b49129c2ba90f7930162b
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Massive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes.

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