Architecture of algae mItochondria translation system and its interplay with mRNA maturation – ARAMIS

Around two billion years ago, the acquisition of mitochondrion, a double membrane-bound endosymbiotic organelle, has dramatically influenced eukaryotic cells evolution. Indeed, mitochondria are central to eukaryotic bioenergetics, with their primary role in ATP generation by oxidative phosphorylation and their important roles in fundamental processes like apoptosis, aging, or development.

Since the establishment of the integrated endosymbiotic bacterium within an ancestral proto-eukaryotic cell, mitochondria have considerably evolved. These organelles now combine bacterial traits inherited from their prokaryote ancestor with distinctive features that evolved during eukaryote history. Their mt gene expression depends on the coordinated expression between the mitochondrial and the nuclear genomes, and consequently, on the interaction between factors of dual prokaryotic and eukaryotic origins.

Several recent results have underlined the extraordinary diversification of mitochondria. Among them, high-resolution structures of mitoribosomes have been obtained for various eukaryotes, revealing tremendous structural differences with bacterial ribosomes and between them. Their architectures show significant variations highlighting an unexpected diversity of mitochondrial translation systems. In particular, the composition and structure of land plant mitoribosomes that has been recently determined is particularly remarkable. As a follow-up to this recent research, deciphering the evolutionary drift of mitochondria in different eukaryotic lineages represents a fascinating challenge. Further studies are thus essential to fully understand the diversity of mt genome expression processes in many unexplored eukaryote lineages.

Here, the ARAMIS project aims at providing detailed mechanistic insights on mt mRNA maturation and translation systems in a prime model organism, the unicellular green alga, Chlamydomonas reinhardtii. Its mt genome possesses remarkable features. All mt mRNAs directly start at the AUG initiation codon and end with post-transcriptionally added poly-cytidine tails, a feature that we recently discovered. Ribosomal RNAs are fragmented and our ongoing characterisation of Chlamydomonas mitoribosome, using single particle cryoEM combined with biochemical and functional studies reveals several peculiarities. We identified a novel small RNA resembling the 5S rRNA and the occurrence of about ten specific novel proteins possessing helical repeat motifs, in particular octotricopeptide repeat proteins.

Based on robust preliminary results and a consortium of four partners with a long-lasting history of fruitful collaborations, characterizing the model alga Chlamydomonas mitochondrial translation apparatus and understanding how its activity is linked with mRNA maturation is the central concern of the ARAMIS project. An integrative analysis performed at the biochemical, genetic, and structural levels will reveal:
- The protein factors associated with mitochondrial mRNA maturation
- The composition, structure, and function of the mitoribosome and the role of novel octotricopeptide repeat proteins
- The molecular mechanisms associated with mitochondrial translation initiation and its interplay with mRNA maturation
As a whole, ARAMIS will be instrumental to understand the biology of mt genome expression in algae. It will thus participate to understand the diversity and evolution of mitochondrial gene expression systems across eukaryotes.