Changes in the transcriptome, ploidy, and optimal light intensity of a cryptomonad upon integration into a kleptoplastic dinoflagellate

Abstract

Endosymbiosis of unicellular eukaryotic algae into previously nonphotosynthetic eukaryotes has established chloroplasts in several eukaryotic lineages. In addition, 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.

Euglenozoan kleptoplasty illuminates the early evolution of photoendosymbiosis

“…using transcriptomics, plastid genomics and time-course observations with transmission electron microscopy in order to evaluate the level of integration between the plastids and the host cell. We demonstrate that R. viridis has no canonical plastids but has only transient kleptoplasts (kP) that have been previously reported also from other systems ( 11 – 18 ) ( SI Appendix , section 1.1 ), which are regularly acquired by consuming Tetraselmis sp. We also show that R. viridis expresses a series of nucleus-encoded proteins with apparent “plastid”-targeting signals that are homologous to those found in the Euglenophyceae and are probably transported into the kleptoplasts.…”

Cytoklepty in the plankton: A host strategy to optimize the bioenergetic machinery of endosymbiotic algae

“…Expansion of the photosynthetic machinery may, therefore, represent a common stepping-stone toward plastid acquisition. Enlarged nuclei and increased genome ploidy, observed here and in several examples of kleptoplastidy, may represent another commonality in plastid acquisition that serves to support photosynthetic expansion (61,62). In other planktonic photosymbioses, it remains unknown whether such morphological transformation and energetic exploitation occur, and the diversity of such relationships merits further investigation using subcellular imaging techniques.…”

Retention of Prey Genetic Material by the Kleptoplastidic Ciliate Strombidium cf. basimorphum

“…This enables Mesodinium species to retain fully functional plastids and live as a complete autotroph for about four generations in the absence of prey (Smith and Hansen, 2007). Such phenomena of kleptoplasty and karyoklepty have been also recorded in some dinoflagellates (Onuma and Horiguchi, 2015;Onuma et al, 2020).…”