Mosaic nature of the mitochondrial proteome: Implications for the origin and evolution of mitochondria

Abstract

Comparative studies of the mitochondrial proteome have identified a conserved core of proteins descended from the α-proteobacterial endosymbiont that gave rise to the mitochondrion and was the source of the mitochondrial genome in contemporary eukaryotes. A surprising result of phylogenetic analyses is the relatively small proportion (10-20%) of the mitochondrial proteome displaying a clear α-proteobacterial ancestry. A large fraction of mitochondrial proteins typically has detectable homologs only in other eukaryotes and is presumed to represent proteins that emerged specifically within eukaryotes. A further significant fraction of the mitochondrial proteome consists of proteins with homologs in prokaryotes, but without a robust phylogenetic signal affiliating them with specific prokaryotic lineages. The presumptive evolutionary source of these proteins is quite different in contending models of mitochondrial origin.

Keywords: endosymbiont; mitochondria; phagotrophy; proteome; syntrophy.

Fig. 1.

Representation of the evolutionary ancestry of the mitochondrial proteome, deduced from phylogenetic-tree reconstructions. Proportions of the four categories vary depending on the organism in question, but the α-proteobacterial component typically constitutes ∼10–20% of the total mitochondrial proteome (8, 32).

Fig. 2.

A schematic view of the preendosymbiont hypothesis. The premitochondrion is seen as a membrane-bound entity endowed with a protein-import system and various ion/small-molecule transporters, compartmentalizing many of the metabolic functions of the mitochondrion. The premitochondrion is assumed to have evolved endogenously within the preeukaryote cell and to contain proteins that would later contribute to the NPC (non–α-proteobacterial component) of the contemporary mitochondrial proteome. An α-proteobacteria–like endosymbiont is converted to the ancestral mitochondrion, effectively “capturing” protein components and functions of the premitochondrion. The endosymbiont contributes the α-proteobacterial component (APC) of the mitochondrial proteome, which is largely directed toward specification of energy-generating capacity in the form of coupled electron transport/oxidative phosphorylation; as well, the mitochondrial inner and outer membranes are assumed to be endosymbiont-derived (57). The conversion of endosymbiont to ancestral mitochondrion is greatly facilitated by the existence of the reservoir of premitochondrial NPC proteins in the host cell. Endosymbiont-to-nucleus gene transfer (EGT), coupled with rationalization of redundant pathways, results in the formation of evolutionarily chimeric enzymatic pathways and protein complexes in the ancestral mitochondrion, as well as functional relocation of the products of some transferred α-proteobacterial genes to other cellular compartments. The premitochondrion is assumed to be a non–energy-generating organelle that imports ATP; a key innovation in the transition to the contemporary mitochondrion is the acquisition of an ADP/ATP transporter that reverses this flow, ultimately allowing the mitochondrion to become the primary site of ATP generation for cellular functions. Modified from ref. .