ArticleProceedings of the National Academy of Sciences of the United States of America2019
A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis.
Article in Proceedings of the National Academy of Sciences of the United States of America, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 38 papers.
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38 citing papers in PubMed, 95 citations in OpenAlex.
- Emergent metabolic parasitism driven by organelle sequestration.Science advances · 2026Article
- Recent plastid replacement in Karlodinium ballantinum (Kareniaceae, Dinoflagellata) challenges the paradigms of endosymbiotic gene transfer.Molecular biology and evolution · 2026Article
- Transient molecular chimerism for exploiting xenogeneic organelles.Nature communications · 2026Article
- Integration and regulation of stolen organelles in a marine protist.The ISME journal · 2026Article
- TheISME communications · 2026Article
- Review
- Genomes of nitrogen-fixing eukaryotes reveal an alternate path for organellogenesis.Proceedings of the National Academy of Sciences of the United States of America · 2025Article
- Long-term functional kleptoplasty in benthic foraminifera.iScience · 2025Article
- Adaptations and metabolic evolution of myzozoan protists across diverse lifestyles and environments.Microbiology and molecular biology reviews : MMBR · 2024Review
- Plastid translocon recycling in dinoflagellates demonstrates the portability of complex plastids between hosts.Current biology : CB · 2024Article
- Interpreting the complexities of the plastid genome in dinoflagellates: a mini-review of recent advances.Plant molecular biology · 2024Review
- Horizontal gene transfer in eukaryotes: aligning theory with data.Nature reviews. Genetics · 2024Review
- New plastids, old proteins: repeated endosymbiotic acquisitions in kareniacean dinoflagellates.EMBO reports · 2024Article
- Intracellular signaling in proto-eukaryotes evolves to alleviate regulatory conflicts of endosymbiosis.PLoS computational biology · 2024Article
- Taming the perils of photosynthesis by eukaryotes: constraints on endosymbiotic evolution in aquatic ecosystems.Communications biology · 2023Review
- Multiple parallel origins of parasitic Marine Alveolates.Nature communications · 2023Article
- Prey preference in a kleptoplastic dinoflagellate is linked to photosynthetic performance.The ISME journal · 2023Article
- Extreme genome diversity and cryptic speciation in a harmful algal-bloom-forming eukaryote.Current biology : CB · 2023Article
- Euglenozoan kleptoplasty illuminates the early evolution of photoendosymbiosis.Proceedings of the National Academy of Sciences of the United States of America · 2023Article
- Food shaped photosynthesis: Photophysiology of the sea slugOpen research Europe · 2023Article
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Authors and funding
3 authors at 2 institutions in 2 countries.
Funding
No grant is acknowledged in the PubMed record.
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.
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