Dinoflagellates with relic endosymbiont nuclei as models for elucidating organellogenesis

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.

Putative genome features of relic green alga-derived nuclei in dinoflagellates and future perspectives as model organisms

“…On the other hand, a previous study on the nucleomorph genomes of both the lineages indicated that EGTs from the nucleomorphs were likely to have already ceased [4]. Recently, we reported two novel nucleomorph-bearing dinoflagellates for the first time in the last 30 years [7]. These two distantly related dinoflagellates, namely MGD and TGD strains, possess the green alga-derived compartment containing a relic nucleus and a plastid.…”

“…Transcriptome analyses revealed that some photosynthesis-related proteins of green algal origin are encoded in both nuclear and nucleomorph genomes. This recent finding suggested that genome reorganization via EGTs in both TGD and MGD is still incomplete [7]. Phylogenetic analyses also indicated that the origins of both endosymbionts are close relatives of a particular green algal genus, Pedinomonas.…”

“…Here, we analyzed the features of nucleomorph genomes in MGD and TGD strains. Since the genomic data of MGD/TGD nucleomorphs are currently unavailable, we revisited the transcriptome data reported by Sarai et al (2020) [7]. As described in the previous study, the transcripts of MGD and TGD, which encode proteins with similarity to green algal proteins, could be divided into two populations comprising low and high G + C% [7].…”

“…Low G + C% composition is a common feature of previously known nucleomorph genomes and other reduced genomes (e.g., mitochondria, plastids, some parasites and bacterial endosymbionts of insects) [6]. The transcripts belonging to the low G + C % population were predicted to be expressed from the nucleomorph genomes [7]. We classified green algal transcripts into two clusters using an unsupervised clustering method based on the G + C% composition and gene expression levels.…”

“…Then, what kind of mysteries would be unveiled by the future works using MGD and TGD systems? One of the advantages of MGD and TGD is that the origins of their endosymbionts have been clearly pinpointed to close relatives of the genus Pedinomonas, while the plastid origins of cryptophytes and chlorarachniophytes were only narrowed down to the phylum/class-level (Rhodophyta and Chlorophyta/ Ulvophyceae, respectively) [7,11]. A comparison between the reduced nucleomorph genomes of the dinoflagellates and that of a closest free-living relative (i.e., Pedinomonas) would allow tracing of the detailed processes involved during the reductive genome evolution in eukaryote-eukaryote endosymbioses.…”