A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis

Hehenberger, Elisabeth, Gast, Rebecca J. and Keeling, Patrick J. (2019) A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis PNAS Proceedings of the National Academy of Sciences of the United States of America, 116 (36). pp. 17934-17942. DOI 10.1073/pnas.1910121116.

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Abstract

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.

Document Type: Article
Additional Information: Data deposition: Raw reads of the transcriptomic analysis have been deposited to NCBI SRA as SRP132912 (RSD) and SRP133243 (Phaeocystis antarctica), as described in SI Appendix, SI Material and Methods. Other: Phylogenetic reconstructions for all trees discussed in the manuscript have been deposited to figshare repositories under the DOIs 10. 6084/m9.figshare.7851467 and 10.6084/m9.figshare.7856864.
Keywords: plastid endosymbiosis; kleptoplasty; dinoflagellates; plastid integration
Research affiliation: OceanRep > GEOMAR > FB3 Marine Ecology > FB3-OEB Ökosystembiologie des Ozeans
Woods Hole
Refereed: Yes
DOI etc.: 10.1073/pnas.1910121116
ISSN: 0027-8424
Date Deposited: 08 Oct 2019 10:43
Last Modified: 08 Oct 2019 10:43
URI: http://eprints.uni-kiel.de/id/eprint/47907

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