Changes in the transcriptome, ploidy, and optimal light intensity of a cryptomonad upon integration into a kleptoplastic dinoflagellate
Ryo Onuma, Shunsuke Hirooka, Yu Kanesaki, Takayuki Fujiwara, Hirofumi Yoshikawa, Shin-ya Miyagishima
The ISME Journal (2020) DOI:10.1038/s41396-020-0693-4
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Endosymbiosis of unicellular eukaryotic algae into previously nonphotosynthetic eukaryotes has established chloroplasts in several eukaryotic lineages. Additionally, certain unicellular organisms in several different lineages ingest algae and utilize them as temporal chloroplasts (kleptoplasts) for weeks to months before digesting them. Among these organisms, the dinoflagellate Nusuttodinium aeruginosum ingests the cryptomonad Chroomonas sp. and enlarges the kleptoplast with the aid of the cryptomonad nucleus. To understand how the cryptomonad nucleus is remodeled in the dinoflagellate, here we examined changes in the transcriptome and ploidy of the ingested nucleus. We show that, after ingestion, genes involved in metabolism, translation, and DNA replication are upregulated while those involved in sensory systems and cell motility are downregulated. In the dinoflagellate cell, the cryptomonad nucleus undergoes polyploidization that correlates with an increase in the mRNA levels of upregulated genes. In addition, the ingested nucleus almost loses transcriptional responses to light. Because polyploidization and loss of transcriptional regulation are also known to have occurred during the establishment of endosymbiotic organelles, these changes are probably a common trend in endosymbiotic evolution. Furthermore, we show that the kleptoplast and dinoflagellate are more susceptible to high light than the free-living cryptomonad but that the ingested nucleus reduces this damage.
Figure: Kleptoplasty in Nusuttodinium aeruginosum.
(A) Micrographs showing the coculture of N. aeruginosum cells with Chroomonas sp.-derived kleptoplasts and free Chroomonas sp. (left). From the coculture, N. aeruginosum cells with the kleptoplasts (middle) were separated from free Chroomonas sp. (right) by filtration. Scale bar = 10 μm.
(B) Micrographs showing the change in the nucleus and kleptoplast derived from Chroomonas sp. in N. aeruginosum cells. Cells were stained with SYBR Green. Images of differential interference contrast (DIC), SYBR Green staining, and kleptoplast red fluorescence (Chl) are shown. The arrowhead indicates a nucleus derived from Chroomonas sp. The cell in the image from day 3 ingested two nuclei. Scale bar = 10 μm.
(C) Schematic comparison of prey–predator, transient endosymbiotic (kleptoplasty), and permanent endosymbiotic relationships. Predators start digesting algae immediately after phagocytic ingestion of algae (left). Kleptoplastic species retain the ingested algae for days to weeks in the cell before digesting them in some cases, including that of N. aeruginosum, with the nucleus of the algae (middle). The present study shows that the ingested nucleus is polyploidized in the host cell, which increases mRNA levels. The ingested nucleus almost loses transcriptional regulation. These changes were also common to the course of establishment of nucleomorph and chloroplast (also other types of plastids) as obligate endosymbionts in eukaryotes (right).