Potential causes and consequences of rapid mitochondrial genome evolution in thermoacidophilic Galdieria (Rhodophyta)

The Cyanidiophyceae is an early-diverged red algal class that thrives in
extreme conditions around acidic hot springs. Although this lineage has
been highlighted as a model for understanding the biology of extremophilic
eukaryotes, little is known about the molecular evolution of their
mitochondrial genomes (mitogenomes). To fill this knowledge gap, we
sequenced five mitogenomes from representative clades of Cyanidiophyceae
and identified two major groups, here referred to as Galdieria-type
(G-type) and Cyanidium-type (C-type). G-type mitogenomes exhibit the
following three features: (i) reduction in genome size and gene inventory,
(ii) evolution of unique protein properties including charge, hydropathy,
stability, amino acid composition, and protein size, and (iii) distinctive
GC-content and skewness of nucleotides. Based on GC-skew-associated
characteristics, we postulate that unidirectional DNA replication may have
resulted in the rapid evolution of G-type mitogenomes. The high
divergence of G-type mitogenomes was likely driven by natural
selection in the multiple extreme environments that Galdieria species
inhabit combined with their highly flexible heterotrophic metabolism. We
speculate that the interplay between mitogenome divergence and adaptation
may help explain the dominance of Galdieria species in diverse extreme
habitats.