Origin of Mitochondria

Background

Mitochondria are eukaryotic organelles that are mainly known for their role as ‘the powerhouses of the cell’, supplying the bulk of energy that the cell demands. Mitochondria are also very interesting from a evolutionary point of view, because they have features that make them very similar to bacteria:

  • A distinct, commonly circular genome, separate from the nuclear genome
  • Genes that are homologous to bacterial genes
  • Outer and inner membrane structure
  • Independent DNA replication and division
  • Similar size and shape as bacteria

 

These similarities have prompted the hypothesis that mitochondria are derived from bacteria, by a process termed endosymbiosis. The first person to recognize mitochondria as descendants of endosymbiotic bacteria was Ivan Wallin in 1926 [1]. After this, the theory fell out of grace, possibly due to the college textbook of E.B. Wilson, who regarded endosymbiotic theories as ‘too fanciful’. It was not until 1967 before the endosymbiotic theory was re-popularized again by the late Lynn Margulis, by a model known as the Serial Endosymbiosis Theory, or SET [2]. Endosymbiotic theory is nowadays generally accepted as the best model for the origin of mitochondria.

SET
Cartoon depicting the Serial Endosymbiosis Theory (SET) proposed by Lynn Margulis in 1967 [2]

So if the mitochondria were derived from the bacteria, what kind of bacterium was this mitochondrial progenitor? Early phylogenetic analyses performed with bacterial and mitochondrial small subunit rRNA (16S rRNA) sequences done by Carl Woese and colleagues in 1985 identified the Alphaproteobacteria as the most likely candidate [3]. Since then, this affiliation has been confirmed many times. It is still unclear however, whích alphaproteobacterial lineage provided the mitochondrial ancestor. While most studies hint towards the Rickettsiales, the oceanic SAR11 and even Rhodospirillales have been suggested as well. In addition, one study has suggested the existence of an oceanic mitochondria affiliated clade (OMAC), based on metagenomic sequence data of Craig Venter’s global oceanic survey (GOS) expedition.

One additional important conclusion that can be drawn from comparative genomics analyses addressing mitochondrial evolution, is that all mitochondria form a monophyletic group. This basically means that all mitochondria and mitochondria-like organelles from all extant eukaryotic lineages can be traced back to a single ancestor. This inherently also implies that mitochondrial endosymbiosis happened only once in eukaryotic evolution. There are several lines of evidence that support monophyly of the mitochondria [4]:

  • All phylogenetic and phylogenomic analyses yield mitochondria as a monophyletic group
  • Genes encoded by mitochondrial genomes are, with a few exceptions, a subset of the most gene rich mitochondria, that of Reclinomonas americana and Andalucia godoyi
  • Ribosomal protein genes are clustered in the same order in the mitochondrial genome as in bacterial genomes. However, some genes in these clusters are missing in mitochondria, and across all eukaryotics, the sáme deletions can be observed

 

Not all eukaryotes harbor the classical aerobic mitochondria. The absence of classic mitochondria in these species led to a hypothesis in which these species, collectively called Archezoa, represent the descendants of a hypothetical lineage coined ‘the proto-eukaryote’. The proto-eukaryote supposedly had all typical eukaryotic features but lacked mitochondria. But it has now been demonstrated that these Archezoa actually contain derived mitochondria, organelles that were once mitochondria in their evolutionary past (anaerobic mitochondria, mitochondria-like organelles, hydrogenosomes and mitosomes) [5]. This consequently suggested that the Last Common Eukaryotic Ancestor (LECA) contained the ancestor of all mitochondria and derived mitochondria and, assuming that true Archezoa have never existed, the acquisition of the mitochondrial ancestor triggered eukaryogenesis. This in turn means that the host in the mitochondrial endosymbiosis must have been a prokaryote.

In summary, it appears that

  1. All mitochondria and mitochondria derived organelles are descendants from a single, alphaproteobacterial ancestor
  2. The acquisition of the mitochondrial endosymbiont triggered eukaryogenesis
  3. The host of the mitochondrial, alphaproteobacterial endosymbiont was a prokaryote

 

Even though the origin of mitochondria in these aspects are quite well understood, several questions remain. What kind of conditions drove the mitochondrial endosymbiosis? What was the nature of this relationship? What was the identity of the host?

The project

These questions all try to figure something out that occurred in the distant past. Therefore you would expect that if you want to answer them, you start looking for fossils or other signs from the past. But actually, the favored method is to look at modern day organisms. By comparing them, it is possible to say something about their common ancestor. Likewise, when we want to say something about the mitochondrial ancestor, we look at modern day mitochondria and Alphaproteobacteria. In this project, we have (partially) sequenced the genome a number of previously unknown Alphaproteobacteria that are candidate members of new alphaproteobacterial lineages. By comparing them with the genomes of known Alphaproteobacteria and mitochondria using phylogenomic methods, we will be able to gain new insights on the nature of the mitochondrial ancestor.