Nuclear and organellar phylogenies provide insights into evolutionary history and species boundaries in Galdieria

Exploration of life in extreme environments allows the discovery of organisms with extraordinary biotechnological potential. Hot springs, characterised by extreme conditions (pH, < 2; Temperature > 40°C; high concentrations of metals), present a formidable challenge for most life forms, yet support a few specialised archaea, bacteria, and eukaryotes, including the unicellular red alga Galdieria. Beyond their ecological relevance, members of the order Galdieriales emerged as promising platforms for biotechnological applications, including metal and rare earth elements (REEs) recovery, bioremediation under extreme conditions, and sustainable biomass production. Previous phylogenetic studies based on plastid and nuclear genes suggested a complex genetic structure within Galdieria, with evidence for multiple diverging clades within the species G. sulphuraria. To resolve these enigmatic relationships, we employed a genome-scale approach, integrating plastid, mitochondrial, and nuclear data from Galdieria strains collected across diverse geographical locations. Our comprehensive phylogenetic analysis revealed divergence of mitochondrial, plastid, and nuclear genomes into at least seven distinct and well-supported clades; alongside i) independent evolutionary trajectories of these genomic lineages, and ii) incongruent interspecies relationships among the three genomes, reflecting complex evolutionary dynamics. Synonymous and non-synonymous substitution analyses further underscored differential evolutionary pressures on the three cellular genomes acting across the Galdieria species, with strong purifying selection in plastid genes and more relaxed selection in mitochondrial and nuclear genomes. In this context, the genetic and evolutionary framework presented here provides a crucial basis for understanding the molecular determinants underlying the exceptional metabolic versatility and stress tolerance that make Galdieriales attractive candidates for applied biotechnology.