A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis
Plastid endosymbiosis has been a major force in the evolution of eukaryotic cellular complexity, but how endosymbionts are integrated is still poorly understood at a mechanistic level. Dinoflagellates, an ecologically important protist lineage, represent a unique model to study this process because...
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Online Access: | https://oceanrep.geomar.de/id/eprint/47907/ https://oceanrep.geomar.de/id/eprint/47907/1/17934.full.pdf https://doi.org/10.1073/pnas.1910121116 |
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ftoceanrep:oai:oceanrep.geomar.de:47907 2023-05-15T13:40:30+02:00 A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis Hehenberger, Elisabeth Gast, Rebecca J. Keeling, Patrick J. 2019-09-03 text https://oceanrep.geomar.de/id/eprint/47907/ https://oceanrep.geomar.de/id/eprint/47907/1/17934.full.pdf https://doi.org/10.1073/pnas.1910121116 en eng National Academy of Sciences https://oceanrep.geomar.de/id/eprint/47907/1/17934.full.pdf Hehenberger, E. , Gast, R. J. and Keeling, P. J. (2019) A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis. Open Access PNAS Proceedings of the National Academy of Sciences of the United States of America, 116 (36). pp. 17934-17942. DOI 10.1073/pnas.1910121116 <https://doi.org/10.1073/pnas.1910121116>. doi:10.1073/pnas.1910121116 info:eu-repo/semantics/openAccess Article PeerReviewed 2019 ftoceanrep https://doi.org/10.1073/pnas.1910121116 2023-04-07T15:47:32Z Plastid endosymbiosis has been a major force in the evolution of eukaryotic cellular complexity, but how endosymbionts are integrated is still poorly understood at a mechanistic level. Dinoflagellates, an ecologically important protist lineage, represent a unique model to study this process because dinoflagellate plastids have repeatedly been reduced, lost, and replaced by new plastids, leading to a spectrum of ages and integration levels. Here we describe deep-transcriptomic analyses of the Antarctic Ross Sea dinoflagellate (RSD), which harbors long-term but temporary kleptoplasts stolen from haptophyte prey, and is closely related to dinoflagellates with fully integrated plastids derived from different haptophytes. In some members of this lineage, called the Kareniaceae, their tertiary haptophyte plastids have crossed a tipping point to stable integration, but RSD has not, and may therefore reveal the order of events leading up to endosymbiotic integration. We show that RSD has retained its ancestral secondary plastid and has partitioned functions between this plastid and the kleptoplast. It has also obtained genes for kleptoplast-targeted proteins via horizontal gene transfer (HGT) that are not derived from the kleptoplast lineage. Importantly, many of these HGTs are also found in the related species with fully integrated plastids, which provides direct evidence that genetic integration preceded organelle fixation. Finally, we find that expression of kleptoplast-targeted genes is unaffected by environmental parameters, unlike prey-encoded homologs, suggesting that kleptoplast-targeted HGTs have adapted to posttranscriptional regulation mechanisms of the host. Article in Journal/Newspaper Antarc* Antarctic Ross Sea OceanRep (GEOMAR Helmholtz Centre für Ocean Research Kiel) Antarctic Ross Sea The Antarctic Proceedings of the National Academy of Sciences 116 36 17934 17942 |
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OceanRep (GEOMAR Helmholtz Centre für Ocean Research Kiel) |
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English |
description |
Plastid endosymbiosis has been a major force in the evolution of eukaryotic cellular complexity, but how endosymbionts are integrated is still poorly understood at a mechanistic level. Dinoflagellates, an ecologically important protist lineage, represent a unique model to study this process because dinoflagellate plastids have repeatedly been reduced, lost, and replaced by new plastids, leading to a spectrum of ages and integration levels. Here we describe deep-transcriptomic analyses of the Antarctic Ross Sea dinoflagellate (RSD), which harbors long-term but temporary kleptoplasts stolen from haptophyte prey, and is closely related to dinoflagellates with fully integrated plastids derived from different haptophytes. In some members of this lineage, called the Kareniaceae, their tertiary haptophyte plastids have crossed a tipping point to stable integration, but RSD has not, and may therefore reveal the order of events leading up to endosymbiotic integration. We show that RSD has retained its ancestral secondary plastid and has partitioned functions between this plastid and the kleptoplast. It has also obtained genes for kleptoplast-targeted proteins via horizontal gene transfer (HGT) that are not derived from the kleptoplast lineage. Importantly, many of these HGTs are also found in the related species with fully integrated plastids, which provides direct evidence that genetic integration preceded organelle fixation. Finally, we find that expression of kleptoplast-targeted genes is unaffected by environmental parameters, unlike prey-encoded homologs, suggesting that kleptoplast-targeted HGTs have adapted to posttranscriptional regulation mechanisms of the host. |
format |
Article in Journal/Newspaper |
author |
Hehenberger, Elisabeth Gast, Rebecca J. Keeling, Patrick J. |
spellingShingle |
Hehenberger, Elisabeth Gast, Rebecca J. Keeling, Patrick J. A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis |
author_facet |
Hehenberger, Elisabeth Gast, Rebecca J. Keeling, Patrick J. |
author_sort |
Hehenberger, Elisabeth |
title |
A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis |
title_short |
A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis |
title_full |
A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis |
title_fullStr |
A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis |
title_full_unstemmed |
A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis |
title_sort |
kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis |
publisher |
National Academy of Sciences |
publishDate |
2019 |
url |
https://oceanrep.geomar.de/id/eprint/47907/ https://oceanrep.geomar.de/id/eprint/47907/1/17934.full.pdf https://doi.org/10.1073/pnas.1910121116 |
geographic |
Antarctic Ross Sea The Antarctic |
geographic_facet |
Antarctic Ross Sea The Antarctic |
genre |
Antarc* Antarctic Ross Sea |
genre_facet |
Antarc* Antarctic Ross Sea |
op_relation |
https://oceanrep.geomar.de/id/eprint/47907/1/17934.full.pdf Hehenberger, E. , Gast, R. J. and Keeling, P. J. (2019) A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis. Open Access PNAS Proceedings of the National Academy of Sciences of the United States of America, 116 (36). pp. 17934-17942. DOI 10.1073/pnas.1910121116 <https://doi.org/10.1073/pnas.1910121116>. doi:10.1073/pnas.1910121116 |
op_rights |
info:eu-repo/semantics/openAccess |
op_doi |
https://doi.org/10.1073/pnas.1910121116 |
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Proceedings of the National Academy of Sciences |
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116 |
container_issue |
36 |
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17934 |
op_container_end_page |
17942 |
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1766136350538465280 |