Hyper-eccentric structural genes in the mitochondrial genome of the algal parasiteHemistasia phaeocysticola

Abstract

Diplonemid mitochondria are considered to have very eccentric structural genes. Coding regions of individual diplonemid mitochondrial genes are fragmented into small pieces and found on different circular DNAs. Short RNAs transcribed from each DNA molecule mature through a unique RNA maturation process involving assembly and three types of RNA editing (i.e., U insertion and A-to-I and C-to-U substitutions), although the molecular mechanism(s) of RNA maturation and the evolutionary history of these eccentric structural genes still remain to be understood. Since the gene fragmentation pattern is generally conserved among the diplonemid species studied to date, it was considered that their structural complexity has plateaued and further gene fragmentation could not occur. Here, we show the mitochondrial gene structure of Hemistasia phaeocysticola, which was recently identified as a member of a novel lineage in diplonemids, by comparison of the mitochondrial DNA sequences with cDNA sequences synthesized from mature mRNA. The genes of H. phaeocysticola are fragmented much more finely than those of other diplonemids studied to date. Furthermore, in addition to all known types of RNA editing, it is suggested that a novel processing step (i.e., secondary RNA insertion) is involved in the RNA maturation in the mitochondria of H. phaeocysticola. Our findings demonstrate the tremendous plasticity of mitochondrial gene structures.

Perfection of eccentricity: Mitochondrial genomes of diplonemids

“…Studies in our laboratory have initially focused on D. papillatum , but more recently, we have also examined four other diplonemids, which together represent all traditionally recognized genera, Diplonema , Rhynchopus , and Hemistasia . Experimental data from the Diplonema / Rhynchopus ( D/R ) clade were generated by us , whereas those from Hemistasia were produced by another research group , but reanalyzed by us in more detail. Thus, the current list of species investigated at the molecular level comprises five species, D. papillatum , D. ambulator , Diplonema sp.…”

Massive mitochondrial DNA content in diplonemid and kinetoplastid protists

“…In order to produce functional mRNAs, the products of these broken genes must be trans ‐spliced into contiguous sequences (often joined by stretches of post‐transcriptionally added uridines) and heavily edited by nucleotide substitutions . In other diplonemid species, the complexity of trans ‐splicing and RNA editing appears even higher than in D. papillatum . The kinetoplastids and diplonemids appear to illustrate parallel evolution of extremely complex mitochondrial RNA processing machineries not seen in other eukaryotes.…”

A Revised Taxonomy of Diplonemids Including the Eupelagonemidae n. fam. and a Type Species, Eupelagonema oceanica n. gen. & sp.

“…; Yabuki et al. ), as well as some curious metabolic and molecular traits (Morales et al. ; Qian and Keeling ).…”

“…The newly described genera are also marine, though their habitats are yet to be clarified (Tashyreva et al 2018a). Some of these diplonemids have been studied mostly due to their relationship to the more famous kinetoplastids, and because of their baroque mitochondrial genome architecture and posttranscriptional editing characteristics (Kiethega et al 2013;Marande et al 2005;Valach et al 2016;Yabuki et al 2016), as well as some curious metabolic and molecular traits (Morales et al 2016;Qian and Keeling 2001). But overall, the group has not been extensively described, with multiple undetermined phylotypes present in environmental molecular surveys (Tashyreva et al 2018a,b).…”