Biology subjects

Miyagishima, S.-y.

Publications and source records attributed to Miyagishima, S.-y..

7 recordsLinked to original sources

bioRxiv2025

Sexual life cycle establishes the unicellular red algae Cyanidiophyceae as a genetically tractable model lineage for eukaryotic evolution

The thermo-acidophilic unicellular algal class Cyanidiophyceae is the earliest-branching lineage in red algae, which diverged from Viridiplantae lineage (green algae and land plants) soon after chloroplast establishment in the common ancestor of Archaeplastida. Cyanidiophyceae possess extremely simple genomes (8.7-17.8 Mb; approximately 4,800- 7,800 genes), and the cell-wall-less, genetically tractable strain Cyanidioschyzon merolae 10D has served as a model organism. However, its unknown sexual life cycle has limited its utility in studies of evolution and genetics. Inspired by the recent discovery of sexual reproduction in the cyanidiophycean genus Galdieria, we identified similar life cycles in the other cyanidiophycean genera Cyanidioschyzon, Cyanidiococcus, and Cyanidium. In these genera, the cell-walled diploid form, exclusively observed in nature, produces a cell-wall-less haploid form when the culture pH is lowered, and both proliferate asexually. In addition, the cell-wall-less Cyanidioschyzon merolae 10D strain has been shown to be a haploid clone that forms a cell-walled diploid through mating with other haploid clones. Building on these findings, we generated high-quality genomic resources with phase-specific transcriptomes and developed genetic manipulation systems using the cell-wall-less haploids of these genera. We further uncovered phase-specific distribution of histone H3 lysine 27 trimethylation linked to haploid- and diploid-specific gene expression, including transcription factors involved in differentiation associated with sexual reproduction in plants. Additionally, biparental inheritance of organelle DNA occurs following isogamous mating of haploid cells but resolves into uniparental inheritance during diploid proliferation. These advances position Cyanidiophyceae as a powerful model lineage for studying early Archaeplastida evolution, the shared mechanisms of photosynthetic eukaryotes, and their environmental adaptation.

plant biology↗

bioRxiv2024

Community-wide interactions sustain life in geothermal spring habitats

We investigated an alga-dominated geothermal spring community in Yellowstone National Park, USA. Our goal was to determine how cells cope with abiotic stressors during diurnal sampling that spanned over two orders of magnitude in solar irradiance. We report a community level response to toxic metal resistance and energy cycling that spans the three domains of life. Arsenic detoxification is accomplished via complementary gene expression by different lineages. Photosynthesis is dominated by Cyanidioschyzon, with the mixotroph, Galdieria, relegated to nighttime heterotrophy. Many key functions, including the cell cycle, are strongly regulated by diurnal light fluctuations. These results demonstrate that biotic interactions are highly structured in extreme habitats. We suggest this was also the case on the early Earth when geothermal springs were cradles of microbial life, prior to the origin of eukaryotes.

evolutionary biology↗

bioRxiv2024

Experimental bleaching of photosymbiotic amoeba revealed strain-dependent differences in algal symbiosis ability.

Photosymbioses, the symbiotic relationships between photosynthetic algal symbionts and non-photosynthetic eukaryotic hosts, are sporadically found in a lot of eukaryotic lineages, but only a few taxa, such as cnidarians and ciliates hosting algal endosymbionts, have been actively studied for a long time. That has hindered understanding the universal mechanisms of the photosymbiosis establishment. Especially in Amoebozoa, only two species, Mayorella viridis and Parachaos zoochlorella, are reported as photosymbiotic in nature, and their mechanisms of establishing symbiotic relationships are still unclear. To investigate the extent to which and how photosymbiotic amoebae depend on the symbiotic relationships, M. viridis were treated with reagents that are known to induce the collapsing of photosymbiotic relationships, or bleaching, in other photosymbiotic species. As a result, we succeeded in artificially removing algal symbionts from host M. viridis cells with an herbicide, 2-amino-3-chloro-1,4-naphthoquinone. The apo-symbiotic state amoeba cells were able to survive and grow to the same extent as the symbiotic state cells when they fed microbial prey, indicating that the algal symbionts are not essential for the host growth under certain conditions. Furthermore, to see whether the photosymbiotic state is reversible, we fed two strains of algal symbionts to the apo-symbiotic amoeba host. The result showed that the apo-symbiotic hosts were able to ingest symbiont cells and re-establish the symbiotic state. The efficiencies of ingesting algal cells were significantly different depending on algal symbiont strains, indicating that different algal strains possess discrete symbiotic abilities to M. viridis. To our knowledge, we provide first insights on the establishment and collapse of photosymbiosis in Amoebozoa, which pave the way to understand the universal mechanism of photosymbiosis utilizing M. viridis as a model system.

evolutionary biology↗

bioRxiv2023

Structure of PSI-LHCI from Cyanidium caldarium provides evolutionary insights into conservation and diversity of red-lineage LHCs

Light-harvesting complexes (LHCs) are diversified among photosynthetic organisms, and their structural variety in photosystem I-LHC (PSI-LHCI) supercomplexes has been shown. However, structural and evolutionary correlations of red-lineage LHCs are unknown. Here we determined a 1.92-[A] resolution cryo-electron microscopic structure of a PSI-LHCI supercomplex isolated from the red alga Cyanidium caldarium RK-1 (NIES-2137) which is an important taxon in the Cyanidiophyceae, and subsequently investigated these correlations through structural comparisons and phylogenetic analysis. The PSI-LHCI structure shows five LHCI subunits together with a PSI-monomer core. The five LHCIs are composed of two Lhcr1s, two Lhcr2s, and one Lhcr3. Phylogenetic analysis of LHCs bound to PSI in red-lineage algae showed clear orthology of LHCs between C. caldarium and Cyanidioschyzon merolae, whereas no orthologous relationships were found between C. caldarium Lhcr1-3 and LHCs in other red-lineage PSI-LHCI structures. These findings provide evolutionary insights into conservation and diversity of red-lineage LHCs associated with PSI.

plant biology↗

bioRxiv2022

Nitrate Assimilation Underlying Kleptoplasty

While photoautotrophic organisms utilize inorganic nitrogen as the nitrogen source, heterotrophic organisms utilize organic nitrogen and thus do not generally have an inorganic nitrogen assimilation pathway. Here we focused on the nitrogen metabolism of Rapaza viridis, a unicellular eukaryote exhibiting kleptoplasty. Although belonging to the lineage of essentially heterotrophic flagellates, R. viridis exploits the photosynthetic products of the kleptoplasts and was therefore suspected to potentially utilize inorganic nitrogen. From the transcriptome data of R. viridis, we identified the gene RvNaRL, which had sequence similarity to nitrate reductases found in plants. Phylogenetic analysis revealed that RvNaRL was acquired by a horizontal gene transfer event. To verify its function of the protein product RvNaRL, we established a RNAi mediated knockdown and a CRISPR-Cas9-mediated knockout experiments for the first time in R. viridis and applied them to this gene. The RvNaRL knockdown and knockout cells exhibited significant growth only when ammonium was supplied but, in contrast to the wild-type cells, no substantial growth when nitrate was supplied. Such arrested growth in absence of ammonium was attributed to impaired amino acid synthesis due to the deficiency of nitrogen supply from the nitrate assimilation pathway; this in turn resulted in the accumulation of excess photosynthetic products in the form of cytosolic polysaccharide grains as observed. These results indicate that RvNaRL is certainly involved in nitrate assimilation by R. viridis. Thus, we infer that R. viridis achieved its advanced kleptoplastic strategy owing to a posteriori acquisition of the nitrate assimilation pathway the horizontal gene transfer.

biochemistry↗

bioRxiv2022

Transposons repressed by H3K27me3 were co-opted as cis-regulatory elements of H3K27me3 controlled protein coding genes during evolution of plants

The mobility of transposable elements (TEs) contributes to evolution of genomes 1,2. Meanwhile, their uncontrolled activity causes genomic instability and therefore expression of TEs is silenced by host genomes 3,4. TEs are marked with DNA and H3K9 methylation that are associated with silencing in flowering plants 5, animals, and fungi 6. Yet, in distantly related eukaryotes TEs are instead marked by H3K27me3 deposited by the Polycomb Repressive Complex 2 (PRC2) 7-11, an epigenetic mark associated with gene silencing in multicellular eukaryotes 12-15. It was therefore proposed that the ancestral activity of PRC2 was the deposition of H3K27me3 to silence TEs 16. To test this hypothesis we obtained mutants deprived of PRC2 activity and used genomics to analyze the role of PRC2 in extant species along the lineage of Archaeplastida. While in the red alga Cyanidioschyzon merolae more TEs than genes were repressed by PRC2, an opposite trend was observed in bryophytes Marchantia polymorpha and Anthoceros agrestis. In the red alga, TEs silenced by H3K27me3 are in subtelomeres but in bryophytes, TEs and genes marked by H3K27me3 form coregulated transcriptional units. The latter trend was also observed in the flowering plant Arabidopsis thaliana, and we identified cis-elements recognised by transcription factors in TEs flanking genes repressed by PRC2. Together with the silencing of TEs by PRC2 in ciliates that diverged early from an ancestor common with Archaeplastida, our findings support the hypothesis that PRC2 deposited H3K27me3 to silence TEs in early lineages of eukaryotes. During evolution, TE fragments marked with H3K27me3 were selected to shape transcriptional regulation that control networks of genes regulated by PRC2. HighlightsH3K27me3 marks a decreasing proportion of TEs during evolution of plants The polycomb repressive complex 2 represses TEs in red algae and bryophytes H3K27me3-marked TEs in flowering plants contain transcription factor binding sites Transcription factors bind TEs and regulate networks of genes controlled by PRC2

evolutionary biology↗

bioRxiv2021

Genome evolution of a non-parasitic secondary heterotroph, the diatom Nitzschia putrida

Secondary loss of photosynthesis is observed across almost all plastid-bearing branches of the eukaryotic tree of life. However, genome-based insights into the transition from a phototroph into a secondary heterotroph have so far only been revealed for parasitic species. Free-living organisms can yield unique insights into the evolutionary consequence of the loss of photosynthesis, as the parasitic lifestyle requires specific adaptations to host environments. Here we report on the diploid genome of the free-living diatom Nitzschia putrida (35 Mbp), a non-photosynthetic osmotroph whose photosynthetic relatives contribute ca. 40% of net oceanic primary production. Comparative analyses with photosynthetic diatoms revealed that a combination of genes loss, the horizontal acquisition of genes involved in organic carbon degradation, a unique secretome and the rapid divergence of conserved gene families involved in cell wall and extracellular metabolism appear to have facilitated the lifestyle of a non-parasitic, free-living secondary heterotroph.

genomics↗