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

The thermo-acidophilic unicellular algal class Cyanidiophyceae diverged from other red algae soon after primary chloroplast acquisition. 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. Here, we show that in the genera Cyanidioschyzon, Cyanidiococcus, and Cyanidium, 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. Cyanidioschyzon merolae 10D is a haploid clone that forms a cell-walled diploid through mating with other haploid clones. In addition, we generated high-quality genomic resources with phase-specific transcriptomes, identified a compact candidate mating-type region, and developed genetic manipulation systems using the cell-wall-less haploids of these genera. We further uncovered phase-specific distributions 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 environmental adaptation.