Extreme Features of the Galdieria sulphuraria Organellar Genomes: A Consequence of Polyextremophily?

Nuclear genome sequencing from extremophilic eukaryotes has revealed clues about the mechanisms of adaptation to extreme environments, but the functional consequences of extremophily on organellar genomes are unknown. To address this issue, we assembled the mitochondrial and plastid genomes from a polyextremophilic red alga, Galdieria sulphuraria strain 074 W, and performed a comparative genomic analysis with other red algae and more broadly across eukaryotes. The mitogenome is highly reduced in size and genetic content and exhibits the highest guanine-cytosine skew of any known genome and the fastest substitution rate among all red algae. The plastid genome contains a large number of intergenic stem-loop structures but is otherwise rather typical in size, structure, and content in comparison with other red algae. We suggest that these unique genomic modifications result not only from the harsh conditions in which Galdieria lives but also from its unusual capability to grow heterotrophically, endolithically, and in the dark. These conditions place additional mutational pressures on the mitogenome due to the increased reliance on the mitochondrion for energy production, whereas the decreased reliance on photosynthesis and the presence of numerous stem-loop structures may shield the plastome from similar genomic stress.