Mitochondria are best known for their role in the generation of ATP by aerobic respiration. Yet, research in the past half century has shown that they perform a much larger suite of functions and that these functions can vary substantially among diverse eukaryotic lineages. Despite this diversity, all mitochondria derive from a common ancestral organelle that originated from the integration of an endosymbiotic alphaproteobacterium into a host cell related to Asgard Archaea. The transition from endosymbiotic bacterium to permanent organelle entailed a massive number of evolutionary changes including the origins of hundreds of new genes and a protein import system, insertion of membrane transporters, integration of metabolism and reproduction, genome reduction, endosymbiotic gene transfer, lateral gene transfer and the retargeting of proteins. These changes occurred incrementally as the endosymbiont and the host became integrated. Although many insights into this transition have been gained, controversy persists regarding the nature of the original endosymbiont, its initial interactions with the host and the timing of its integration relative to the origin of other features of eukaryote cells. Since the establishment of the organelle, proteins have been gained, lost, transferred and retargeted as mitochondria have specialized into the spectrum of functional types seen across the eukaryotic tree of life.
Mitochondria are eukaryotic organelles that originated from an endosymbiotic α-proteobacterium. As an adaptation to maximize ATP production through oxidative phosphorylation, mitochondria contain inner membrane invaginations called cristae. Recent work has characterized a multi-protein complex in yeast and animal mitochondria called MICOS (mitochondrial contact site and cristae organizing system), responsible for the determination and maintenance of cristae [1-4]. However, the origin and evolution of these characteristic mitochondrial features remain obscure. We therefore conducted a comprehensive search for MICOS components across the major groups that encompass eukaryotic diversity to determine the extent of conservation of this complex. We detected homologs for the majority of MICOS components among opisthokonts (the group containing animals and fungi), but only Mic60 and Mic10 were consistently identified outside this group. The conservation of Mic60 and Mic10 in eukaryotes is consistent with their central role in MICOS function [5-7], indicating that the basic mechanism for cristae determination arose early in evolution and has remained relatively unchanged. We found that eukaryotes with ultrastructurally simplified anaerobic mitochondria that lack cristae have also lost MICOS. We then searched for a prokaryotic MICOS and identified a homolog of Mic60 present only in α-proteobacteria, providing evidence for the endosymbiotic origin of mitochondrial cristae. Our study clarifies the origins of mitochondrial cristae and their subsequent evolutionary history, provides evidence for a general mechanism of cristae formation and maintenance in eukaryotes, and points to a new potential factor involved in membrane differentiation in prokaryotes.
The Alphaproteobacteria is an extraordinarily diverse and ancient group of bacteria. Previous attempts to infer its deep phylogeny have been plagued with methodological artefacts. To overcome this, we analyzed a dataset of 200 single-copy and conserved genes and employed diverse strategies to reduce compositional artefacts. Such strategies include using novel dataset-specific profile mixture models and recoding schemes, and removing sites, genes and taxa that are compositionally biased. We show that the Rickettsiales and Holosporales (both groups of intracellular parasites of eukaryotes) are not sisters to each other, but instead, the Holosporales has a derived position within the Rhodospirillales. A synthesis of our results also leads to an updated proposal for the higher-level taxonomy of the Alphaproteobacteria. Our robust consensus phylogeny will serve as a framework for future studies that aim to place mitochondria, and novel environmental diversity, within the Alphaproteobacteria.
Determining the phylogenetic origin of mitochondria is key to understanding the ancestral mitochondrial symbiosis and its role in eukaryogenesis. However, the precise evolutionary relationship between mitochondria and their closest bacterial relatives remains hotly debated. The reasons include pervasive phylogenetic artefacts, as well as limited protein and taxon sampling. Here, we developed a new model of protein evolution that accommodates both across-site and across-branch compositional heterogeneity.We applied this site-and-branch-heterogeneous model (MAM60+GFmix) to a considerably expanded dataset that comprises 108 mitochondrial proteins of alphaproteobacterial origin, and novel metagenomeassembled genomes from microbial mats, microbialites, and sediments. The MAM60+GFmix model fits the data much better and agrees with analyses of compositionally homogenized datasets with conventional site-heterogenous models. The consilience of evidence thus suggests that mitochondria is sister to the Alphaproteobacteria to the exclusion of MarineProteo1 and Magnetococcia. We also show that the ancestral presence of a crista-developing MICOS complex (a Mitofilin domain-containing Mic60) supports this relationship.
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