Characterization and Comparative Analyses of Mitochondrial Genomes in Single-Celled Eukaryotes to Shed Light on the Diversity and Evolution of Linear Molecular Architecture

Abstract

Determination and comparisons of complete mitochondrial genomes (mitogenomes) are important to understand the origin and evolution of mitochondria. Mitogenomes of unicellular protists are particularly informative in this regard because they are gene-rich and display high structural diversity. Ciliates are a highly diverse assemblage of protists and their mitogenomes (linear structure with high A+T content in general) were amongst the first from protists to be characterized and have provided important insights into mitogenome evolution. Here, we report novel mitogenome sequences from three representatives (Strombidium sp., Strombidium cf. sulcatum, and Halteria grandinella) in two dominant ciliate lineages. Comparative and phylogenetic analyses of newly sequenced and previously published ciliate mitogenomes were performed and revealed a number of important insights. We found that the mitogenomes of these three species are linear molecules capped with telomeric repeats that differ greatly among known species. The genomes studied here are highly syntenic, but larger in size and more gene-rich than those of other groups. They also all share an AT-rich tandem repeat region which may serve as the replication origin and modulate initiation of bidirectional transcription. More generally we identified a split version of ccmf, a cytochrome c maturation-related gene that might be a derived character uniting taxa in the subclasses Hypotrichia and Euplotia. Finally, our mitogenome comparisons and phylogenetic analyses support to reclassify Halteria grandinella from the subclass Oligotrichia to the subclass Hypotrichia. These results add to the growing literature on the unique features of ciliate mitogenomes, shedding light on the diversity and evolution of their linear molecular architecture.

Complete mitochondrial genome of Perilla frutescens (Lamiaceae) insights into structure, Codon usage, repeats, and RNA editing

“…Genomic comparisons and Ka/Ks analysis of protein-coding genes provide a good theoretical basis for exploring the evolution of the Mitochondrial genome 67,68 . Generally, few protein-coding genes in this study were affected by positive selection, which is similar to existing research reports 6,62,65,69,70 . The Ka/Ks analysis of the Mitochondrial genome indicates that widely present PCGs (protein-coding genes) in Mitochondrial are retained.…”

Comparative Genome Analysis Reveals Cis-Regulatory Elements on Gene-Sized Chromosomes of Ciliated Protists

“…For spirotrichous ciliates including Oxytricha , Stylonychia , Uroleptopsis , Euplotes and Strombidium , this fragmentation is extensive, resulting in a MAC genome composed of more than 10,000 telomere-capped chromosomes ( Steinbrück et al, 1981 ; Prescott, 2000 ; Swart et al, 2013 ; Zheng et al, 2018 ; Chen et al, 2019 ; Li et al, 2021 ). These linear nanochromosomes are usually smaller than mitochondrial chromosomes and can carry one or few genes and can be few hundred base pairs up to several kilobases in size ( Swart et al, 2013 ; Zhang et al, 2021 ). These general features make spirotrichous ciliates excellent models to study chromosomal architecture and functions ( Zhao et al, 2021 ; Zheng et al, 2021 ).…”

The Genome of the Mitochondrion-Related Organelle in Cepedea longa, a Large Endosymbiotic Opalinid Inhabiting the Recta of Frogs

“…We speculate that the IGR between tRNA Asp and rps13 genes is the most likely origin of replication, as there are five tandem repeat units with 100 bp each in this region, which we called central tandem repeats, and the direction of gene transcription and GC skew values switch from this region. The central tandem repeats were also found in ciliates with linear mitochondrial genomes (e.g., species in Spirotricha), and they are probably associated with replication and transcription initiation [ 49 , 50 ]. We speculate that the central tandem repeats of C. longa might play an important role in the direction of gene transcription.…”