Extremophiles, while typically bacteria and archaea, are also found in the eukaryotic domain of life. The eukaryote Galdieria sulphuraria is a thermoacidophilic red alga belonging to the class Cyanidiophyceae, an especially unique class as it comprises the basal clade of eukaryotic extremophiles. Galdieria species can grow both photosynthetically and heterotrophically on a variety of carbon sources, thriving down to pH 0 and temperatures up to 56 ˚C, while tolerating high levels of reactive oxygen species and high levels of heavy metals. Here we report whole-genome sequencing of three G. sulphuraria strains, uncovering a compact (13.1 Mb to 16.0 Mb) nuclear genome with 72 to 73 chromosomes, dependent on the strain. Comparative analyses of the macro synteny revealed significant structural rearrangement between G. sulphuraria isolates and the genome shows signs of sexual recombination. This, along with the large number of nuclear chromosomes compared to the genome size, reveals a mechanism of intrinsic adaptability in this eukaryotic extremophile, uncovering how G. sulphuraria can thrive in a rapidly changing extreme environment.

Exploration of life in extreme environments allows the discovery of intriguing organisms with extraordinary biotechnological potential. An example of extreme environments is represented by hot springs, where harsh conditions (pH < 1; Temperature > 50C; high concentrations of metals) are prohibitive for most living organisms, except for archaea, bacteria and a few eukaryotes like the unicellular red alga Galdieria. Phylogenetic analysis based on a few plastid and nuclear genes highlighted the intricate genetic structure of Galdieria and the hypothesis of diverging clades within the G. sulphuraria species. To resolve enigmatic relationships between lineages, we used plastid, mitochondrial and nuclear genome-scale data obtained from numerous strains from around the world. The resulting phylogenomic analysis identified: i) the divergence of each of the mitochondrial, plastid, and nuclear genomes into the same six clear lineages; ii) the independent evolution of the lineages; iii) the incongruent interlineages relationships between the three genomes. Differential evolutionary pressure between the strains and the genomes were also highlighted by synonymous and non-synonymous substitutions.