Diurnal Transcriptional Regulation of Endosymbiotically Derived Genes in the ChlorarachniophyteBigelowiella natans

Abstract

Chlorarachniophyte algae possess complex plastids acquired by the secondary endosymbiosis of a green alga, and the plastids harbor a relict nucleus of the endosymbiont, the so-called nucleomorph. Due to massive gene transfer from the endosymbiont to the host, many proteins involved in plastid and nucleomorph are encoded by the nuclear genome. Genome sequences have provided a blueprint for the fate of endosymbiotically derived genes; however, transcriptional regulation of these genes remains poorly understood. To gain insight into the evolution of endosymbiotic genes, we performed genome-wide transcript profiling along the cell cycle of the chlorarachniophyte Bigelowiella natans, synchronized by light and dark cycles. Our comparative analyses demonstrated that transcript levels of 7,751 nuclear genes (35.7% of 21,706 genes) significantly oscillated along the diurnal/cell cycles, and those included 780 and 147 genes for putative plastid and nucleomorph-targeted proteins, respectively. Clustering analysis of those genes revealed the existence of transcriptional networks related to specific biological processes such as photosynthesis, carbon metabolism, translation, and DNA replication. Interestingly, transcripts of many plastid-targeted proteins in B. natans were induced before dawn, unlike other photosynthetic organisms. In contrast to nuclear genes, 99% nucleomorph genes were found to be constitutively expressed during the cycles. We also found that the nucleomorph DNA replication would be controlled by a nucleus-encoded viral-like DNA polymerase. The results of this study suggest that nucleomorph genes have lost transcriptional regulation along the diurnal cycles, and nuclear genes exert control over the complex plastid including the nucleomorph.

Origin of exon skipping-rich transcriptomes in animals driven by evolution of gene architecture

“…Finally, our analysis of F ES , sp levels in the chlorarachniophyte Bigelowiella natans showed contradictory results. The analysis of two recent transcriptomic datasets [ 42 , 43 ] showed significantly lower ES frequencies than those reported in the original genome paper [ 36 ] (Additional file 1 : Figure S7; p < 1e − 16, Wilcoxon rank-sum test). The reasons behind these differences remain elusive.…”

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

“…In the cryptophyte Guillardia theta , cell-cycle-regulated genes, which are specifically transcribed at certain cell-cycle stages in free-living eukaryotes, are constantly expressed from a nucleomorph (a descendant of a red algal endosymbiont) regardless of its replication or division cycle [ 49 ]. In the chlorarachniophyte Bigelowiella natans , the mRNA levels of almost all of the genes of the nucleomorph (a descendant of a green algal endosymbiont) remained constant throughout a 12-h-light and 12-h-dark cycle [ 50 ]. The loss or reduction of the transcriptional response to light is also applicable to endosymbiotic evolution of organelles from cyanobacterial endosymbionts.…”

Transcriptome Profiling of Bigelowiella natans in Response to Light Stress

“…Suzuki et al. () found the nucleomorph gene, cpn60, expression increased during the dark phase of the diurnal cycle. In our study, cpn60 significantly increase expression under VL, but it did not meet our 1 LFC threshold.…”

“…Suzuki et al. () examined the transcriptional regulation during light/dark cycles in B. natans and observed more than a thousand genes that fluctuated during the diurnal/cell division cycles. Only two of these genes, however, were encoded by the nucleomorph, suggesting a limited role for the nucleomorph in controlling diurnal cycles.…”