Dinoflagellates with relic endosymbiont nuclei as models for elucidating organellogenesis
- 24 February 2020
- journal article
- research article
- Published by Proceedings of the National Academy of Sciences in Proceedings of the National Academy of Sciences of the United States of America
- Vol. 117 (10), 5364-5375
- https://doi.org/10.1073/pnas.1911884117
Abstract
Nucleomorphs are relic endosymbiont nuclei so far found only in two algal groups, cryptophytes and chlorarachniophytes, which have been studied to model the evolutionary process of integrating an endosymbiont alga into a host-governed plastid (organellogenesis). However, past studies suggest that DNA transfer from the endosymbiont to host nuclei had already ceased in both cryptophytes and chlorarachniophytes, implying that the organellogenesis at the genetic level has been completed in the two systems. Moreover, we have yet to pinpoint the closest free-living relative of the endosymbiotic alga engulfed by the ancestral chlorarachniophyte or cryptophyte, making it difficult to infer how organellogenesis altered the endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which endosymbiont-to-host DNA transfer is on-going and for which endosymbiont/plastid origins can be inferred at a fine taxonomic scale. Here, we report two previously undescribed dinoflagellates, strains MGD and TGD, with green algal endosymbionts enclosing plastids as well as relic nuclei (nucleomorphs). We provide evidence for the presence of DNA in the two nucleomorphs and the transfer of endosymbiont genes to the host (dinoflagellate) genomes. Furthermore, DNA transfer between the host and endosymbiont nuclei was found to be in progress in both the MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the endosymbionts at the genus level. With the combined evidence, we conclude that the host–endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as models for elucidating organellogenesis.Keywords
This publication has 89 references indexed in Scilit:
- Full-length transcriptome assembly from RNA-Seq data without a reference genomeNature Biotechnology, 2011
- Aligning Short Sequencing Reads with BowtieCurrent Protocols in Bioinformatics, 2010
- A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastidsProceedings of the National Academy of Sciences of the United States of America, 2010
- Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiationNature Biotechnology, 2010
- Protein targeting into secondary plastids of chlorarachniophytesProceedings of the National Academy of Sciences of the United States of America, 2009
- Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and functionProceedings of the National Academy of Sciences of the United States of America, 2007
- Spliced leader RNA trans-splicing in dinoflagellatesProceedings of the National Academy of Sciences of the United States of America, 2007
- RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed modelsBioinformatics, 2006
- Complete nucleotide sequence of the chlorarachniophyte nucleomorph: Nature’s smallest nucleusProceedings of the National Academy of Sciences of the United States of America, 2006
- Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomesNature Reviews Genetics, 2004