Perfection of eccentricity: Mitochondrial genomes of diplonemids

Abstract

Mitochondria are the sandbox of evolution as exemplified most particularly by the diplonemids, a group of marine microeukaryotes. These protists are uniquely characterized by their highly multipartite mitochondrial genome and systematically fragmented genes whose pieces are spread out over several dozens of chromosomes. The type species Diplonema papillatum was the first member of this group in which the expression of fragmented mitochondrial genes was investigated experimentally. We now know that gene expression involves separate transcription of gene pieces (modules), RNA editing of module transcripts, and module joining to mature mRNAs and rRNAs. The mechanism of cognate module recognition and ligation is distinct from known intron splicing and remains to be uncovered. Here, we review the current status of research on mitochondrial genome architecture, as well as gene complement, structure, and expression modes in diplonemids. Further, we discuss the potential molecular mechanisms of posttranscriptional processing, and finally reflect on the evolutionary trajectories and trends of mtDNA evolution as seen in this protist group. © 2018 IUBMB Life, 70(12):1197Life, 70(12): -1206Life, 70(12): , 2018

The draft nuclear genome sequence and predicted mitochondrial proteome of Andalucia godoyi, a protist with the most gene-rich and bacteria-like mitochondrial genome

“…Finally, in the context of mitochondrial genome and proteome evolution, it is striking that on the one hand Discoba contains the least derived, most bacteria-like mitochondrial genomes yet described (within jakobids), and on the other hand, some of the most highly derived, least bacteria-like mitochondrial genomes known (within euglenozoans [216,217]. Comparison of jakobid and euglenozoan mitochondrial proteomes, as they become available, will be an important tool for tracing post-LECA mitochondrial evolution within and between these specific clades.…”

Mitochondrial genetics revisited

“…This eccentric genetic component of eukaryotic cells exhibits a great architectural diversity across the tree of life (Smith & Keeling, ), and although the numerous mitochondrial genomes now sequenced give us an impression of exhaustive knowledge (http://www.ncbi.nlm.nih.gov/genome.organelle/), new surprises are not excluded as novel evolutionary branches will be explored. For example, it was recently discovered that Diplonemids synthesise mitochondrial products similar to that of other organisms by a complex bottom‐up assembly of short RNA modules independently transcribed from multiple DNA molecules in absence of conventional genes ( Burger & Valach, ) .…”

Evolutionary mitochondrial biology in titisee

“…The articles by Burger and Valach and Lukeš et al , among numerous other reports in the literature, serve to emphasize the incredible variety of ways, some quite bizarre, in which mitochondrial genes can be encoded and expressed. These observations give the impression that the mitochondrion is a molecular biological playground, able to find very different solutions to the problem of organellar genetic information flow in different eukaryotes.…”

“…Two articles in this issue graphically illustrate the exceptional variability in structure and expression that characterizes mitochondrial DNA (mtDNA) across the diversity of eukaryotes. Burger and Valach review the extraordinary organization of the mitochondrial genome in diplonemids, which together with euglenids and kinetoplastids comprise Euglenozoa. This clade, which exhibits some of the most unusual patterns of mitochondrial genome organization and expression uncovered to date , is a member of a eukaryotic supergroup that also contains the most gene‐rich, bacteria‐like and least derived mitochondrial genomes yet described .…”

“…Module transcripts are trans‐spliced to form translatable mRNAs, a process that also involves a limited amount of 3′‐U addition and, for some transcripts, substantial C‐to‐U and A‐to‐I editing. The mechanisms by which this complicated mitochondrial mRNA processing occurs, and the enzymatic machinery mediating it, remain to be elucidated .…”