Nucleomorph and plastid genome sequences of the chlorarachniophyte Lotharella oceanica: convergent reductive evolution and frequent recombination in nucleomorph-bearing algae
Identifieur interne : 000194 ( Main/Exploration ); précédent : 000193; suivant : 000195Nucleomorph and plastid genome sequences of the chlorarachniophyte Lotharella oceanica: convergent reductive evolution and frequent recombination in nucleomorph-bearing algae
Auteurs : Goro Tanifuji ; Naoko T. Onodera ; Matthew W. Brown [États-Unis] ; Bruce A. Curtis ; Andrew J. Roger ; Gane Ka-Shu Wong ; Michael Melkonian [Allemagne] ; John M. ArchibaldSource :
- BMC Genomics [ 1471-2164 ] ; 2014.
Abstract
Nucleomorphs are residual nuclei derived from eukaryotic endosymbionts in chlorarachniophyte and cryptophyte algae. The endosymbionts that gave rise to nucleomorphs and plastids in these two algal groups were green and red algae, respectively. Despite their independent origin, the chlorarachniophyte and cryptophyte nucleomorph genomes share similar genomic features such as extreme size reduction and a three-chromosome architecture. This suggests that similar reductive evolutionary forces have acted to shape the nucleomorph genomes in the two groups. Thus far, however, only a single chlorarachniophyte nucleomorph and plastid genome has been sequenced, making broad evolutionary inferences within the chlorarachniophytes and between chlorarachniophytes and cryptophytes difficult. We have sequenced the nucleomorph and plastid genomes of the chlorarachniophyte
The
We have provided insight into the process of nucleomorph genome evolution by elucidating the fine-scale dynamics of sub-telomeric repeat regions. Homologous recombination at the chromosome ends appears to be frequent, serving to expand and contract nucleomorph genome size. The main factor influencing nucleomorph genome size variation between different chlorarachniophyte species appears to be expansion-contraction of these telomere-associated repeats rather than changes in the number of unique protein coding genes. The dynamic nature of chlorarachniophyte nucleomorph genomes lies in stark contrast to their plastid genomes, which appear to be highly stable in terms of gene content and synteny.
The online version of this article (doi:10.1186/1471-2164-15-374) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/1471-2164-15-374
PubMed: 24885563
PubMed Central: 4035089
Affiliations:
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Nucleomorph and plastid genome sequences of the chlorarachniophyte <italic>Lotharella oceanica</italic>: convergent reductive evolution and frequent recombination in nucleomorph-bearing algae</title><author><name sortKey="Tanifuji, Goro" sort="Tanifuji, Goro" uniqKey="Tanifuji G" first="Goro" last="Tanifuji">Goro Tanifuji</name><affiliation><nlm:aff id="Aff1">Department of Biochemistry and Molecular Biology, Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Dalhousie University, Halifax, Nova Scotia B3H 4R2 Canada</nlm:aff><wicri:noCountry code="subfield">Nova Scotia B3H 4R2 Canada</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">Faculty of life and environmental sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8577 Japan</nlm:aff><wicri:noCountry code="subfield">Ibaraki 305-8577 Japan</wicri:noCountry></affiliation></author><author><name sortKey="Onodera, Naoko T" sort="Onodera, Naoko T" uniqKey="Onodera N" first="Naoko T" last="Onodera">Naoko T. Onodera</name><affiliation><nlm:aff id="Aff1">Department of Biochemistry and Molecular Biology, Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Dalhousie University, Halifax, Nova Scotia B3H 4R2 Canada</nlm:aff><wicri:noCountry code="subfield">Nova Scotia B3H 4R2 Canada</wicri:noCountry></affiliation></author><author><name sortKey="Brown, Matthew W" sort="Brown, Matthew W" uniqKey="Brown M" first="Matthew W" last="Brown">Matthew W. Brown</name><affiliation wicri:level="1"><nlm:aff id="Aff3">Department of Biological Sciences, Mississippi State University, Mississippi State Mississippi, 39762 USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, Mississippi State University, Mississippi State Mississippi</wicri:regionArea><wicri:noRegion>Mississippi State Mississippi</wicri:noRegion></affiliation></author><author><name sortKey="Curtis, Bruce A" sort="Curtis, Bruce A" uniqKey="Curtis B" first="Bruce A" last="Curtis">Bruce A. Curtis</name><affiliation><nlm:aff id="Aff1">Department of Biochemistry and Molecular Biology, Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Dalhousie University, Halifax, Nova Scotia B3H 4R2 Canada</nlm:aff><wicri:noCountry code="subfield">Nova Scotia B3H 4R2 Canada</wicri:noCountry></affiliation></author><author><name sortKey="Roger, Andrew J" sort="Roger, Andrew J" uniqKey="Roger A" first="Andrew J" last="Roger">Andrew J. Roger</name><affiliation><nlm:aff id="Aff1">Department of Biochemistry and Molecular Biology, Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Dalhousie University, Halifax, Nova Scotia B3H 4R2 Canada</nlm:aff><wicri:noCountry code="subfield">Nova Scotia B3H 4R2 Canada</wicri:noCountry></affiliation></author><author><name sortKey="Ka Shu Wong, Gane" sort="Ka Shu Wong, Gane" uniqKey="Ka Shu Wong G" first="Gane" last="Ka-Shu Wong">Gane Ka-Shu Wong</name><affiliation><nlm:aff id="Aff4">Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9 Canada</nlm:aff><wicri:noCountry code="subfield">AB T6G 2E9 Canada</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff5">Department of Medicine, University of Alberta, Edmonton, AB T6G 2E1 Canada</nlm:aff><wicri:noCountry code="subfield">AB T6G 2E1 Canada</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff6">BGI-Shenzhen, Beishan Industrial Zone, Yantian District, Shenzhen 518083 China</nlm:aff><wicri:noCountry code="subfield">Shenzhen 518083 China</wicri:noCountry></affiliation></author><author><name sortKey="Melkonian, Michael" sort="Melkonian, Michael" uniqKey="Melkonian M" first="Michael" last="Melkonian">Michael Melkonian</name><affiliation wicri:level="1"><nlm:aff id="Aff7">Department of Botany, Cologne Biocenter, University of Cologne, Cologne, 50674 Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Botany, Cologne Biocenter, University of Cologne, Cologne</wicri:regionArea><wicri:noRegion>Cologne</wicri:noRegion><wicri:noRegion>Cologne</wicri:noRegion><wicri:noRegion>Cologne</wicri:noRegion></affiliation></author><author><name sortKey="Archibald, John M" sort="Archibald, John M" uniqKey="Archibald J" first="John M" last="Archibald">John M. Archibald</name><affiliation><nlm:aff id="Aff1">Department of Biochemistry and Molecular Biology, Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Dalhousie University, Halifax, Nova Scotia B3H 4R2 Canada</nlm:aff><wicri:noCountry code="subfield">Nova Scotia B3H 4R2 Canada</wicri:noCountry></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24885563</idno><idno type="pmc">4035089</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4035089</idno><idno type="RBID">PMC:4035089</idno><idno type="doi">10.1186/1471-2164-15-374</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000167</idno><idno type="wicri:Area/Pmc/Curation">000167</idno><idno type="wicri:Area/Pmc/Checkpoint">000182</idno><idno type="wicri:Area/Ncbi/Merge">000527</idno><idno type="wicri:Area/Ncbi/Curation">000527</idno><idno type="wicri:Area/Ncbi/Checkpoint">000527</idno><idno type="wicri:Area/Main/Merge">000194</idno><idno type="wicri:Area/Main/Curation">000194</idno><idno type="wicri:Area/Main/Exploration">000194</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Nucleomorph and plastid genome sequences of the chlorarachniophyte <italic>Lotharella oceanica</italic>: convergent reductive evolution and frequent recombination in nucleomorph-bearing algae</title><author><name sortKey="Tanifuji, Goro" sort="Tanifuji, Goro" uniqKey="Tanifuji G" first="Goro" last="Tanifuji">Goro Tanifuji</name><affiliation><nlm:aff id="Aff1">Department of Biochemistry and Molecular Biology, Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Dalhousie University, Halifax, Nova Scotia B3H 4R2 Canada</nlm:aff><wicri:noCountry code="subfield">Nova Scotia B3H 4R2 Canada</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff2">Faculty of life and environmental sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8577 Japan</nlm:aff><wicri:noCountry code="subfield">Ibaraki 305-8577 Japan</wicri:noCountry></affiliation></author><author><name sortKey="Onodera, Naoko T" sort="Onodera, Naoko T" uniqKey="Onodera N" first="Naoko T" last="Onodera">Naoko T. Onodera</name><affiliation><nlm:aff id="Aff1">Department of Biochemistry and Molecular Biology, Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Dalhousie University, Halifax, Nova Scotia B3H 4R2 Canada</nlm:aff><wicri:noCountry code="subfield">Nova Scotia B3H 4R2 Canada</wicri:noCountry></affiliation></author><author><name sortKey="Brown, Matthew W" sort="Brown, Matthew W" uniqKey="Brown M" first="Matthew W" last="Brown">Matthew W. Brown</name><affiliation wicri:level="1"><nlm:aff id="Aff3">Department of Biological Sciences, Mississippi State University, Mississippi State Mississippi, 39762 USA</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biological Sciences, Mississippi State University, Mississippi State Mississippi</wicri:regionArea><wicri:noRegion>Mississippi State Mississippi</wicri:noRegion></affiliation></author><author><name sortKey="Curtis, Bruce A" sort="Curtis, Bruce A" uniqKey="Curtis B" first="Bruce A" last="Curtis">Bruce A. Curtis</name><affiliation><nlm:aff id="Aff1">Department of Biochemistry and Molecular Biology, Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Dalhousie University, Halifax, Nova Scotia B3H 4R2 Canada</nlm:aff><wicri:noCountry code="subfield">Nova Scotia B3H 4R2 Canada</wicri:noCountry></affiliation></author><author><name sortKey="Roger, Andrew J" sort="Roger, Andrew J" uniqKey="Roger A" first="Andrew J" last="Roger">Andrew J. Roger</name><affiliation><nlm:aff id="Aff1">Department of Biochemistry and Molecular Biology, Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Dalhousie University, Halifax, Nova Scotia B3H 4R2 Canada</nlm:aff><wicri:noCountry code="subfield">Nova Scotia B3H 4R2 Canada</wicri:noCountry></affiliation></author><author><name sortKey="Ka Shu Wong, Gane" sort="Ka Shu Wong, Gane" uniqKey="Ka Shu Wong G" first="Gane" last="Ka-Shu Wong">Gane Ka-Shu Wong</name><affiliation><nlm:aff id="Aff4">Department of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9 Canada</nlm:aff><wicri:noCountry code="subfield">AB T6G 2E9 Canada</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff5">Department of Medicine, University of Alberta, Edmonton, AB T6G 2E1 Canada</nlm:aff><wicri:noCountry code="subfield">AB T6G 2E1 Canada</wicri:noCountry></affiliation><affiliation><nlm:aff id="Aff6">BGI-Shenzhen, Beishan Industrial Zone, Yantian District, Shenzhen 518083 China</nlm:aff><wicri:noCountry code="subfield">Shenzhen 518083 China</wicri:noCountry></affiliation></author><author><name sortKey="Melkonian, Michael" sort="Melkonian, Michael" uniqKey="Melkonian M" first="Michael" last="Melkonian">Michael Melkonian</name><affiliation wicri:level="1"><nlm:aff id="Aff7">Department of Botany, Cologne Biocenter, University of Cologne, Cologne, 50674 Germany</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Botany, Cologne Biocenter, University of Cologne, Cologne</wicri:regionArea><wicri:noRegion>Cologne</wicri:noRegion><wicri:noRegion>Cologne</wicri:noRegion><wicri:noRegion>Cologne</wicri:noRegion></affiliation></author><author><name sortKey="Archibald, John M" sort="Archibald, John M" uniqKey="Archibald J" first="John M" last="Archibald">John M. Archibald</name><affiliation><nlm:aff id="Aff1">Department of Biochemistry and Molecular Biology, Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Dalhousie University, Halifax, Nova Scotia B3H 4R2 Canada</nlm:aff><wicri:noCountry code="subfield">Nova Scotia B3H 4R2 Canada</wicri:noCountry></affiliation></author></analytic><series><title level="j">BMC Genomics</title><idno type="eISSN">1471-2164</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>Nucleomorphs are residual nuclei derived from eukaryotic endosymbionts in chlorarachniophyte and cryptophyte algae. The endosymbionts that gave rise to nucleomorphs and plastids in these two algal groups were green and red algae, respectively. Despite their independent origin, the chlorarachniophyte and cryptophyte nucleomorph genomes share similar genomic features such as extreme size reduction and a three-chromosome architecture. This suggests that similar reductive evolutionary forces have acted to shape the nucleomorph genomes in the two groups. Thus far, however, only a single chlorarachniophyte nucleomorph and plastid genome has been sequenced, making broad evolutionary inferences within the chlorarachniophytes and between chlorarachniophytes and cryptophytes difficult. We have sequenced the nucleomorph and plastid genomes of the chlorarachniophyte <italic>Lotharella oceanica</italic> in order to gain insight into nucleomorph and plastid genome diversity and evolution.</p></sec><sec><title>Results</title><p>The <italic>L. oceanica</italic> nucleomorph genome was found to consist of three linear chromosomes totaling ~610 kilobase pairs (kbp), much larger than the 373 kbp nucleomorph genome of the model chlorarachniophyte <italic>Bigelowiella natans</italic>. The <italic>L. oceanica</italic> plastid genome is 71 kbp in size, similar to that of <italic>B. natans</italic>. Unexpectedly long (~35 kbp) sub-telomeric repeat regions were identified in the <italic>L. oceanica</italic> nucleomorph genome; internal multi-copy regions were also detected. Gene content analyses revealed that nucleomorph house-keeping genes and spliceosomal intron positions are well conserved between the <italic>L. oceanica</italic> and <italic>B. natans</italic> nucleomorph genomes. More broadly, gene retention patterns were found to be similar between nucleomorph genomes in chlorarachniophytes and cryptophytes. Chlorarachniophyte plastid genomes showed near identical protein coding gene complements as well as a high level of synteny.</p></sec><sec><title>Conclusions</title><p>We have provided insight into the process of nucleomorph genome evolution by elucidating the fine-scale dynamics of sub-telomeric repeat regions. Homologous recombination at the chromosome ends appears to be frequent, serving to expand and contract nucleomorph genome size. The main factor influencing nucleomorph genome size variation between different chlorarachniophyte species appears to be expansion-contraction of these telomere-associated repeats rather than changes in the number of unique protein coding genes. The dynamic nature of chlorarachniophyte nucleomorph genomes lies in stark contrast to their plastid genomes, which appear to be highly stable in terms of gene content and synteny.</p></sec><sec><title>Electronic supplementary material</title><p>The online version of this article (doi:10.1186/1471-2164-15-374) contains supplementary material, which is available to authorized users.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Dolezal, P" uniqKey="Dolezal P">P Dolezal</name></author><author><name sortKey="Likic, V" uniqKey="Likic V">V Likic</name></author><author><name sortKey="Tachezy, J" uniqKey="Tachezy J">J Tachezy</name></author><author><name sortKey="Lithgow, T" uniqKey="Lithgow T">T Lithgow</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gray, Mw" uniqKey="Gray M">MW Gray</name></author><author><name sortKey="Burger, G" uniqKey="Burger G">G Burger</name></author><author><name 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uniqKey="Horsnell T">T Horsnell</name></author><author><name sortKey="Rice, P" uniqKey="Rice P">P Rice</name></author><author><name sortKey="Rajandream, Ma" uniqKey="Rajandream M">MA Rajandream</name></author><author><name sortKey="Barrell, B" uniqKey="Barrell B">B Barrell</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Schattner, P" uniqKey="Schattner P">P Schattner</name></author><author><name sortKey="Brooks, An" uniqKey="Brooks A">AN Brooks</name></author><author><name sortKey="Lowe, Tm" uniqKey="Lowe T">TM Lowe</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Renner, T" uniqKey="Renner T">T Renner</name></author><author><name sortKey="Waters, Er" uniqKey="Waters E">ER Waters</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Katoh, K" uniqKey="Katoh K">K Katoh</name></author><author><name sortKey="Standley, Dm" uniqKey="Standley D">DM Standley</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Capella Gutierrez, S" uniqKey="Capella Gutierrez S">S Capella-Gutierrez</name></author><author><name sortKey="Silla Martinez, Jm" uniqKey="Silla Martinez J">JM Silla-Martinez</name></author><author><name sortKey="Gabaldon, T" uniqKey="Gabaldon T">T Gabaldon</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Criscuolo, A" uniqKey="Criscuolo A">A Criscuolo</name></author><author><name sortKey="Gribaldo, S" uniqKey="Gribaldo S">S Gribaldo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Brown, Mw" uniqKey="Brown M">MW Brown</name></author><author><name sortKey="Sharpe, Sc" uniqKey="Sharpe S">SC Sharpe</name></author><author><name sortKey="Silberman, Jd" uniqKey="Silberman J">JD Silberman</name></author><author><name sortKey="Heiss, Aa" uniqKey="Heiss A">AA Heiss</name></author><author><name sortKey="Lang, Bf" uniqKey="Lang B">BF Lang</name></author><author><name sortKey="Simpson, Agb" uniqKey="Simpson A">AGB Simpson</name></author><author><name sortKey="Roger, Aj" uniqKey="Roger A">AJ Roger</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Burki, F" uniqKey="Burki F">F Burki</name></author><author><name sortKey="Shalchian Tabrizi, K" uniqKey="Shalchian Tabrizi K">K Shalchian-Tabrizi</name></author><author><name sortKey="Minge, M" uniqKey="Minge M">M Minge</name></author><author><name sortKey="Skjaeveland, A" uniqKey="Skjaeveland A">A Skjaeveland</name></author><author><name sortKey="Nikolaev, Si" uniqKey="Nikolaev S">SI Nikolaev</name></author><author><name sortKey="Jakobsen, Ks" uniqKey="Jakobsen K">KS Jakobsen</name></author><author><name sortKey="Pawlowski, J" uniqKey="Pawlowski J">J Pawlowski</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Burki, F" uniqKey="Burki F">F Burki</name></author><author><name sortKey="Okamoto, N" uniqKey="Okamoto N">N Okamoto</name></author><author><name sortKey="Pombert, Jf" uniqKey="Pombert J">JF Pombert</name></author><author><name sortKey="Keeling, Pj" uniqKey="Keeling P">PJ Keeling</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hampl, V" uniqKey="Hampl V">V Hampl</name></author><author><name sortKey="Hug, L" uniqKey="Hug L">L Hug</name></author><author><name sortKey="Leigh, Jw" uniqKey="Leigh J">JW Leigh</name></author><author><name sortKey="Dacks, Jb" uniqKey="Dacks J">JB Dacks</name></author><author><name sortKey="Lang, Bf" uniqKey="Lang B">BF Lang</name></author><author><name sortKey="Simpson, Agb" uniqKey="Simpson A">AGB Simpson</name></author><author><name sortKey="Roger, Aj" uniqKey="Roger A">AJ Roger</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Brown, Mw" uniqKey="Brown M">MW Brown</name></author><author><name sortKey="Kolisko, M" uniqKey="Kolisko M">M Kolisko</name></author><author><name sortKey="Silberman, Jd" uniqKey="Silberman J">JD Silberman</name></author><author><name sortKey="Roger, Aj" uniqKey="Roger A">AJ Roger</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Allemagne</li><li>États-Unis</li></country></list><tree><noCountry><name sortKey="Archibald, John M" sort="Archibald, John M" uniqKey="Archibald J" first="John M" last="Archibald">John M. Archibald</name><name sortKey="Curtis, Bruce A" sort="Curtis, Bruce A" uniqKey="Curtis B" first="Bruce A" last="Curtis">Bruce A. Curtis</name><name sortKey="Ka Shu Wong, Gane" sort="Ka Shu Wong, Gane" uniqKey="Ka Shu Wong G" first="Gane" last="Ka-Shu Wong">Gane Ka-Shu Wong</name><name sortKey="Onodera, Naoko T" sort="Onodera, Naoko T" uniqKey="Onodera N" first="Naoko T" last="Onodera">Naoko T. Onodera</name><name sortKey="Roger, Andrew J" sort="Roger, Andrew J" uniqKey="Roger A" first="Andrew J" last="Roger">Andrew J. Roger</name><name sortKey="Tanifuji, Goro" sort="Tanifuji, Goro" uniqKey="Tanifuji G" first="Goro" last="Tanifuji">Goro Tanifuji</name></noCountry><country name="États-Unis"><noRegion><name sortKey="Brown, Matthew W" sort="Brown, Matthew W" uniqKey="Brown M" first="Matthew W" last="Brown">Matthew W. Brown</name></noRegion></country><country name="Allemagne"><noRegion><name sortKey="Melkonian, Michael" sort="Melkonian, Michael" uniqKey="Melkonian M" first="Michael" last="Melkonian">Michael Melkonian</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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