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Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

Identifieur interne : 000153 ( France/Analysis ); précédent : 000152; suivant : 000154

Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

Auteurs : Jean-François Flot [Allemagne] ; Boris Hespeels [Belgique] ; Xiang Li [Belgique] ; Benjamin Noel [France] ; Irina Arkhipova [États-Unis] ; Etienne G. J. Danchin [France] ; Andreas Hejnol [Norvège] ; Bernard Henrissat [France] ; Romain Koszul [France] ; Jean-Marc Aury [France] ; Valerie Barbe [France] ; Roxane-Marie Barthelemy [France] ; Jens Bast

Source :

RBID : Hal:hal-01282538

English descriptors

Abstract

Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years1. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing2. However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873)3, and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.


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DOI: 10.1038/nature12326


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<orgName type="acronym">CEA</orgName>
<desc>
<address>
<addrLine>Centre de SaclayCentre de GrenobleCentre de Cadaracheetc</addrLine>
<country key="FR"></country>
</address>
<ref type="url">http://www.cea.fr/</ref>
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<orgName>Université Paris-Saclay</orgName>
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<address>
<addrLine>Espace Technologique, Bat. Discovery - RD 128 - 2e ét., 91190 Saint-Aubin</addrLine>
<country key="FR"></country>
</address>
<ref type="url">https://www.universite-paris-saclay.fr/fr</ref>
</desc>
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</tutelle>
</tutelles>
</hal:affiliation>
<country>France</country>
</affiliation>
</author>
<author>
<name sortKey="Barbe, Valerie" sort="Barbe, Valerie" uniqKey="Barbe V" first="Valerie" last="Barbe">Valerie Barbe</name>
<affiliation wicri:level="1">
<hal:affiliation type="laboratory" xml:id="struct-55375" status="VALID">
<orgName>Genoscope - Centre national de séquençage [Evry]</orgName>
<orgName type="acronym">GENOSCOPE</orgName>
<desc>
<address>
<addrLine>2, rue Gaston Crémieux CP5706 91057 EVRY Cedex</addrLine>
<country key="FR"></country>
</address>
<ref type="url">http://www.genoscope.cns.fr</ref>
</desc>
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<idno type="RNSR">201622496M</idno>
<orgName>Direction de Recherche Fondamentale (CEA)</orgName>
<orgName type="acronym">DRF (CEA)</orgName>
<date type="start">2016-01-01</date>
<desc>
<address>
<addrLine>Direction de Recherche FondamentaleFundamental Research DivisionCEA Saclay91191 Gif-sur-Yvette</addrLine>
<country key="FR"></country>
</address>
<ref type="url">http://ceasciences.fr/</ref>
</desc>
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<orgName>Commissariat à l'énergie atomique et aux énergies alternatives</orgName>
<orgName type="acronym">CEA</orgName>
<desc>
<address>
<addrLine>Centre de SaclayCentre de GrenobleCentre de Cadaracheetc</addrLine>
<country key="FR"></country>
</address>
<ref type="url">http://www.cea.fr/</ref>
</desc>
</org>
</tutelle>
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<orgName>Université Paris-Saclay</orgName>
<desc>
<address>
<addrLine>Espace Technologique, Bat. Discovery - RD 128 - 2e ét., 91190 Saint-Aubin</addrLine>
<country key="FR"></country>
</address>
<ref type="url">https://www.universite-paris-saclay.fr/fr</ref>
</desc>
</org>
</tutelle>
</tutelles>
</hal:affiliation>
<country>France</country>
</affiliation>
</author>
<author>
<name sortKey="Barthelemy, Roxane Marie" sort="Barthelemy, Roxane Marie" uniqKey="Barthelemy R" first="Roxane-Marie" last="Barthelemy">Roxane-Marie Barthelemy</name>
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<date type="end">2013-12-31</date>
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<address>
<country key="FR"></country>
</address>
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<orgName>École Centrale de Marseille</orgName>
<orgName type="acronym">ECM</orgName>
<date type="start">2006-09-27</date>
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<address>
<addrLine>Pôle de l'étoile - Technopole de Château-Gombert - 38 rue Frédéric Joliot-Curie - 13013 Marseille</addrLine>
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<idno type="IdRef">15863621X</idno>
<idno type="ISNI">0000 0001 2176 4817</idno>
<orgName>Aix Marseille Université</orgName>
<orgName type="acronym">AMU</orgName>
<date type="start">2012-01-01</date>
<desc>
<address>
<addrLine>Aix-Marseille UniversitéJardins du Pharo58 Boulevard Charles Livon13284 Marseille cedex 7</addrLine>
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<idno type="IdRef">02636817X</idno>
<idno type="ISNI">0000000122597504</idno>
<orgName>Centre National de la Recherche Scientifique</orgName>
<orgName type="acronym">CNRS</orgName>
<date type="start">1939-10-19</date>
<desc>
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</address>
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</desc>
</org>
</tutelle>
</tutelles>
</hal:affiliation>
<country>France</country>
<placeName>
<settlement type="city">Marseille</settlement>
<region type="region" nuts="2">Provence-Alpes-Côte d'Azur</region>
</placeName>
<orgName type="university">Université d'Aix-Marseille</orgName>
</affiliation>
</author>
<author>
<name sortKey="Bast, Jens" sort="Bast, Jens" uniqKey="Bast J" first="Jens" last="Bast">Jens Bast</name>
</author>
</analytic>
<idno type="DOI">10.1038/nature12326</idno>
<series>
<title level="j">Nature</title>
<idno type="ISSN">0028-0836</idno>
<imprint>
<date type="datePub">2013-08-22</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass>
<keywords scheme="mix" xml:lang="en">
<term> asexual evolution</term>
<term> bdelloid rotifer</term>
<term> genome</term>
<term>Adineta vaga</term>
</keywords>
</textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<p>Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years1. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing2. However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873)3, and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.</p>
</div>
</front>
</TEI>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>Belgique</li>
<li>France</li>
<li>Norvège</li>
<li>États-Unis</li>
</country>
<region>
<li>Provence-Alpes-Côte d'Azur</li>
</region>
<settlement>
<li>Marseille</li>
</settlement>
<orgName>
<li>Université d'Aix-Marseille</li>
</orgName>
</list>
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<noCountry>
<name sortKey="Bast, Jens" sort="Bast, Jens" uniqKey="Bast J" first="Jens" last="Bast">Jens Bast</name>
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<noRegion>
<name sortKey="Flot, Jean Francois" sort="Flot, Jean Francois" uniqKey="Flot J" first="Jean-François" last="Flot">Jean-François Flot</name>
</noRegion>
</country>
<country name="Belgique">
<noRegion>
<name sortKey="Hespeels, Boris" sort="Hespeels, Boris" uniqKey="Hespeels B" first="Boris" last="Hespeels">Boris Hespeels</name>
</noRegion>
<name sortKey="Li, Xiang" sort="Li, Xiang" uniqKey="Li X" first="Xiang" last="Li">Xiang Li</name>
</country>
<country name="France">
<noRegion>
<name sortKey="Noel, Benjamin" sort="Noel, Benjamin" uniqKey="Noel B" first="Benjamin" last="Noel">Benjamin Noel</name>
</noRegion>
<name sortKey="Aury, Jean Marc" sort="Aury, Jean Marc" uniqKey="Aury J" first="Jean-Marc" last="Aury">Jean-Marc Aury</name>
<name sortKey="Barbe, Valerie" sort="Barbe, Valerie" uniqKey="Barbe V" first="Valerie" last="Barbe">Valerie Barbe</name>
<name sortKey="Barthelemy, Roxane Marie" sort="Barthelemy, Roxane Marie" uniqKey="Barthelemy R" first="Roxane-Marie" last="Barthelemy">Roxane-Marie Barthelemy</name>
<name sortKey="Danchin, Etienne G J" sort="Danchin, Etienne G J" uniqKey="Danchin E" first="Etienne G. J." last="Danchin">Etienne G. J. Danchin</name>
<name sortKey="Henrissat, Bernard" sort="Henrissat, Bernard" uniqKey="Henrissat B" first="Bernard" last="Henrissat">Bernard Henrissat</name>
<name sortKey="Koszul, Romain" sort="Koszul, Romain" uniqKey="Koszul R" first="Romain" last="Koszul">Romain Koszul</name>
</country>
<country name="États-Unis">
<noRegion>
<name sortKey="Arkhipova, Irina" sort="Arkhipova, Irina" uniqKey="Arkhipova I" first="Irina" last="Arkhipova">Irina Arkhipova</name>
</noRegion>
</country>
<country name="Norvège">
<noRegion>
<name sortKey="Hejnol, Andreas" sort="Hejnol, Andreas" uniqKey="Hejnol A" first="Andreas" last="Hejnol">Andreas Hejnol</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>

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