The pre-endosymbiont hypothesis: A new perspective on the origin and evolution of mitochondria

Abstract

Mitochondrial DNA (mtDNA) is unquestionably the remnant of an a-proteobacterial genome, yet only 10%-20% of mitochondrial proteins are demonstrably a-proteobacterial in origin (the "a-proteobacterial component," or APC). The evolutionary ancestry of the nona- proteobacterial component (NPC) is obscure and not adequately accounted for in current models of mitochondrial origin. I propose that in the host cell that accommodated an aproteobacterial endosymbiont, much of the NPC was already present, in the form of a membrane-bound metabolic organelle (the premitochondrion) that compartmentalized many of the non-energy-generating functions of the contemporary mitochondrion. I suggest that this organelle also possessed a protein import system and various ion and small-molecule transporters. In such a scenario, an a-proteobacterial endosymbiont could have been converted relatively directly and rapidly into an energy-generating organelle that incorporated the extant metabolic functions of the premitochondrion. This model (the "preendosymbiont hypothesis") effectively represents a synthesis of previous, contending mitochondrial origin hypotheses, with the bulk of the mitochondrial proteome (much of the NPC) having an endogenous origin and the minority component (the APC) having a xenogenous origin. © 2014 Cold Spring Harbor Laboratory Press; all rights reserved.