A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis
© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the National Academy of Sciences.of the United States of America 116(36), (2019): 17934-17942, doi:10.1073/pnas.1910121116. Plastid e...
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ftwhoas:oai:darchive.mblwhoilibrary.org:1912/24678 2023-05-15T13:48:31+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 https://hdl.handle.net/1912/24678 unknown National Academy of Sciences https://doi.org/10.1073/pnas.1910121116 Hehenberger, E., Gast, R. J., & Keeling, P. J. (2019). A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis. Proceedings of the National Academy of Sciences of the United States of America, 116(36), 17934-17942. https://hdl.handle.net/1912/24678 doi:10.1073/pnas.1910121116 Attribution-NonCommercial-NoDerivatives 4.0 International http://creativecommons.org/licenses/by-nc-nd/4.0/ CC-BY-NC-ND Hehenberger, E., Gast, R. J., & Keeling, P. J. (2019). A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis. Proceedings of the National Academy of Sciences of the United States of America, 116(36), 17934-17942. doi:10.1073/pnas.1910121116 plastid endosymbiosis kleptoplasty dinoflagellates plastid integration Article 2019 ftwhoas https://doi.org/10.1073/pnas.1910121116 2022-05-28T23:03:17Z © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the National Academy of Sciences.of the United States of America 116(36), (2019): 17934-17942, doi:10.1073/pnas.1910121116. 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. We are grateful to Martin Kolisko and Fabien Burki for ... Article in Journal/Newspaper Antarc* Antarctic Ross Sea Woods Hole Scientific Community: WHOAS (Woods Hole Open Access Server) Antarctic Ross Sea The Antarctic Proceedings of the National Academy of Sciences 116 36 17934 17942 |
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Open Polar |
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Woods Hole Scientific Community: WHOAS (Woods Hole Open Access Server) |
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ftwhoas |
language |
unknown |
topic |
plastid endosymbiosis kleptoplasty dinoflagellates plastid integration |
spellingShingle |
plastid endosymbiosis kleptoplasty dinoflagellates plastid integration Hehenberger, Elisabeth Gast, Rebecca J. Keeling, Patrick J. A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis |
topic_facet |
plastid endosymbiosis kleptoplasty dinoflagellates plastid integration |
description |
© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the National Academy of Sciences.of the United States of America 116(36), (2019): 17934-17942, doi:10.1073/pnas.1910121116. 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. We are grateful to Martin Kolisko and Fabien Burki for ... |
format |
Article in Journal/Newspaper |
author |
Hehenberger, Elisabeth Gast, Rebecca J. Keeling, Patrick J. |
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://hdl.handle.net/1912/24678 |
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_source |
Hehenberger, E., Gast, R. J., & Keeling, P. J. (2019). A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis. Proceedings of the National Academy of Sciences of the United States of America, 116(36), 17934-17942. doi:10.1073/pnas.1910121116 |
op_relation |
https://doi.org/10.1073/pnas.1910121116 Hehenberger, E., Gast, R. J., & Keeling, P. J. (2019). A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis. Proceedings of the National Academy of Sciences of the United States of America, 116(36), 17934-17942. https://hdl.handle.net/1912/24678 doi:10.1073/pnas.1910121116 |
op_rights |
Attribution-NonCommercial-NoDerivatives 4.0 International http://creativecommons.org/licenses/by-nc-nd/4.0/ |
op_rightsnorm |
CC-BY-NC-ND |
op_doi |
https://doi.org/10.1073/pnas.1910121116 |
container_title |
Proceedings of the National Academy of Sciences |
container_volume |
116 |
container_issue |
36 |
container_start_page |
17934 |
op_container_end_page |
17942 |
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1766249361349541888 |