Potential causes and consequences of rapid mitochondrial genome evolution in thermoacidophilic Galdieria (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 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. Conclusions 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.

Comparison of Aspergillus chevalieri and related species in dark tea at different aspects: Morphology, enzyme activity and mitochondrial genome

“…However, the G-C skew was different from the four Aspergillus species, except A. cristatum. Moreover, it showed a relatively strong preference for the C-base and that result was consistent with the study conducted by Cho et al (2020), who reported that there was a certain correlation of base skew with the geographical location and environmental pressure of the species. It was speculated that this difference was attributed to the directional mutation of the mitochondrial DNA of A. chevalieri and A. cristatum, as the dominant bacteria of dark tea fermentation, under the long-term influence of a special environment.…”

Resolving Complexities in Taxonomic Lineages of the Organellar and Nuclear Genomes of Galdieria through Comparative Phylogenomic Analysis

“…Mitochondrial genomes features, such as genome size, number of CDS, synteny and high CG content are shared by all the isolates and consistent with those described in previous works [69,70]. As stated by Jain et al in 2015, the high GC skew could be a consequence of the heterotrophic life of G. sulphuraria, which requires an increase of the energy request from mitochondria when it finds itself living endolithically and in the dark [69].…”

“…For instance, the longest noncoding and most variable region in animal mitochondrial DNA is identified as Control Region (CR) and comprises a third strand of DNA, creating a D-loop [71]. In vertebrates this region has strand-specific bias and is involved in the asymmetric DNA replication mechanism [70,72].…”

Genome-wide signatures of adaptation to extreme environments in red algae

“…Highly diverged genomic features between Galdieriales and Cyanidiales species also likely resulted in phenotypic differences (e.g., size, shape, and organelle features) and local adaptation to microhabitats 19 . Galdieriales occupies a more diverse variety of niches in extreme environments (e.g., mine drainage sites, endolithic environments) than do Cyanidiales species, whose habitats (e.g., ditches and streams near hot springs) may be more ecologically stable 13 , 42 .…”

“…Several lines of evidence (e.g., phylogeny, morphological traits, ecological habitats, and energy production systems) suggest that the Cyanidiophyceae is divided into two major orders, the Cyanidiales and Galdieriales (previously Cyanidiaceae and Galdieriaceae) 18 , 19 . Draft genome assemblies are currently available for 14 cyanidiophyceans: one strain of Cyanidioschyzon merolae , two strains of Cyanidiococcus yangmingshanensis , nine strains of Galdieria sulphuraria , and two strains of Galdieria phlegrea 9 , 14 , 15 , 20 , 21 .…”