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

Abstract

Background 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). Results To fill this knowledge gap, we sequenced five mitogenomes from representative clades of Cyanidiophyceae and identified two major groups, here referred to asGaldieria-type (G-type) andCyanidium-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 ofG-type mitogenomes. Conclusions The high divergence ofG-type mitogenomes was likely driven by natural selection in the multiple extreme environments thatGaldieria species inhabit combined with their highly flexible heterotrophic metabolism. We speculate that the interplay between mitogenome divergence and adaptation may help explain the dominance ofGaldieria species in diverse extreme habitats.