The Origin and Diversification of Mitochondria

Abstract

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.

Why the Lipid Divide? Membrane Proteins as Drivers of the Split between the Lipids of the Three Domains of Life

“…I suggest that the choice was due to the increasing reliance of eukaryotes on (proto)mitochondrial ATP production (among multiple other functions), which is driven largely by a host of ancestrally bacterial membrane proteins closely associated with the bacterial‐like membrane.…”

“…The core topology of the tree of life remains contentious, but evidence amassed over the last decade supports the view that eukaryotes as we presently know them arose from a merger of prokaryotic cells, involving an archaeal host (likely from within the recently described Asgard superphylum) and an endosymbiotic bacterium (likely from a lineage within or closely related to the modern Alphaproteobacteria) . If this was the case, eukaryotes likely inherited their membrane lipids from their prokaryotic forebears.…”

Fe–S cluster assembly in the supergroup Excavata

“…The intimate relationship between eukaryotic cells and mitochondria, as endosymbiont-derived organelles, has taken billion of years to establish [1, 2]. It was initially accepted that the basis for the presence of mitochondria in virtually every eukaryotic cell had been the provision of energy from their oxidative phosphorylation machinery, yet several lines of evidence have proven otherwise [3].…”

“…The description of various types of mitochondria and mitochondria-related organelles (or MRO), many of which are found in a spectrum of unrelated protist clades, has brought into the spotlight an enormous organellar diversity, or what is rather a continuum, ranging from a minimalistic MRO of Giardia to the highly complex mitochondria of trypanosomes [4]. MROs have been found in eukaryotic supergroups Excavata, SAR (stramenopiles/alveolates/Rhizaria), photosynthetic algae, and Opisthokonta [1, 5]. Organelles of mitochondrial origin, of which MROs form a part, have been classified into five types [5]: (1) “classical mitochondrion” with a complete electron transport chain, which is capable of using oxygen as an electron acceptor, and produces metabolic energy from such machinery; (2 and 3) organelles that bear a functional electron transport chain, yet use other electron acceptors such as fumarate, and are capable of performing both substrate-level phosphorylation and may or may not produce H 2 ; (4) double membrane-bound MROs called hydrogenosomes that are capable of ATP production in anaerobic or microaerophilic environments and excrete H 2 as one of the end products of substrate-level phosphorylation in an organelle lacking electron transport chain [6]; finally, (5) mitosomes represent a type of MRO incapable of energy production, as they lack the components of an active electron chain and mostly have lost their genome [1, 5].…”

Debating Eukaryogenesis—Part 1: Does Eukaryogenesis Presuppose Symbiosis Before Uptake?

“…The cell biologists favor a more protracted process in which the “host” cell incrementally develops many defining eukaryotic traits in the absence of the future endosymbiont, which will allow its uptake by phagocytic‐like mechanisms: autogenesis. [ 3–6 ] By “autogenesis” I do not mean that all organelles are inventions of the eukaryotic cell (the mitochondrion clearly is not), but that most, if not all, of its defining cellular structures evolved in the absence of selective pressures derived from endosymbiont entry. To avoid confusion, let me stress the following.…”