Skip to content

The origin and early evolution of mitochondria (Gray et al., 2001)

This review gives good insight in mainstream theories about mitochondrial evolution. There are a lot of examples that argue for a eukaryotic origin, although differently explained here. It still strikes me how easily organisms are classified into derived or ancient. Interesting examples on the jakobids, that have the largest genome and which contains all other mitochindrial genomes to the exception of one, which has an additional gene which is attributed to nucleus to mitochondria transfer. Also interesting is the emergence of striking parallels in phylogenetic trees separately reconstructed from genes encoded by nuclear DNA and mtDNA, more in line with the eukaryotic origin, I’d think!

I refer to the article for other references to the reasoning for an endosymiotic origin, but most arguments are against it 1) nuclear and mito DNA give similar Trees, 2) Reclomanas and mitochondria seems both highly derived. i.e. they have many differences, 3) ATP production is quite different (see below), 4) gene comparisons show that the yeast mitochondrial genome contains a pot-pourri of genes (see below), 5) it seems that genes were clustered rather to function than assumed descent, 6) eukaryotic genes were recruited from the nucleus in order to make sense out of the data, 7. article called ‘the mosaic nature of the eukaryotic nucleus’.

Two comprehensive mitochondrial genome-sequencing programs have particularly targeted mtDNA in protists [17] and fungi [18]. A number of specific and general insights into mitochondrial genome evolution follow from these data. The first is that ATP production, coupled to electron transport, and translation of mitochondrial proteins represent the essence of mitochondrial function: these functions are common to all mitochondrial genomes and can be traced unambiguously and directly to an α-proteobacterial ancestor. The mitochondrial genome encodes essential components for both of these processes [8,9].

The second insight is that the most ancestral (least derived), most bacterium-like and most gene-rich mitochondrial genome yet described is the 69,034 base pair (bp) mtDNA of the protist Reclinomonas americana, a jakobid flagellate [19] (jakobids are a group of putatively early diverging protozoa that share ultrastructural features with certain amitochondrial protists). By comparison, some other protist mtDNAs, most fungal, and all animal mtDNAs are highly derived, having diverged away from the ancestral pattern exemplified by R. americana mtDNA.

Mitochondrial gene content varies widely, from a high of 67 protein-coding genes in R. americana mtDNA to only three in the mitochondrial genome of apicomplexans [8,9], a group of strictly parasitic protists (specific relatives of dinoflagellates) including such organisms as Plasmodium falciparum, the causative agent of malaria. Differential gene content in mtDNAs is attributable primarily to mitochondrion-to-nucleus gene transfer [8,9,10,21,22] (which is demonstrably an on-going process in certain lineages, notably flowering plants [23]). Mitochondrial DNA may also lose genes whose functions are substituted for by unrelated genes encoded in the nucleus. A notable example is the replacement of an original multi-subunit bacteria-like RNA polymerase (inherited from the proto-mitochondrial ancestor and still encoded in certain jakobid - but no other - mitochondrial genomes) by a single-subunit bacteriophage T3/T7-like RNA polymerase, which directs mitochondrial transcription in virtually all eukaryotes [24]. Conversely, there may be complete loss of particular mitochondrial genes (and hence the corresponding functions) without functional complementation by nuclear genes. The complex I (nad) genes of the respiratory chain are one example of such loss. In the yeast Saccharomyces cerevisiae, neither the mitochondrial nor the nuclear genome contains classical complex I genes [25]; their disappearance from yeast mtDNA results in the absence of the first coupling site in the yeast electron-transport chain.

Furthermore, genome sequencing shows that the mitochondrial genome (and therefore mitochondria per se) arose only once in evolution. Several observations support this contention [8,9,10]. First, in any particular mitochondrial genome (with few exceptions [26]), genes that have an assigned function are a subset of those found in R. americana mtDNA. Second, in a number of cases, mitochondrial protein-coding clusters retain the gene order of their bacterial homologs, but these clusters exhibit mitochondrion-specific deletions that are most parsimoniously explained as having occurred in a common ancestor of mitochondrial genomes, subsequent to its divergence from the bacterial ancestor. Third, mitochondria form a monophyletic assemblage to the exclusion of bacterial species in phylogenetic reconstructions using concatenated protein sequences [8,9,25,27,28] as well in small-subunit rRNA trees [12].

A final insight from mitochondrial genome sequencing is the emergence of striking parallels in phylogenetic trees separately reconstructed from genes encoded by nuclear DNA [7] and mtDNA [8,9]. In both cases, certain clades (such as animals plus fungi or red plus green algae) have become robust, although connections among these clades and other eukaryotic species or groups cannot yet be precisely resolved. These emerging parallels support the view that mitochondrial and nuclear genomes have evolved in concert throughout much, if not most, of the evolutionary history of the domain Eukarya.

A second consideration is that although mitochondria and R. prowazekii exhibit very similar functional profiles with respect to ATP production (reflecting the common evolutionary origin of their electron transport chains), associated aspects of ATP utilization are quite different. For example, whereas mitochondria export ATP to the cytosol, Rickettsia uses the ATP it produces, and even imports ATP from the host during early stages in its development [29]. The membrane-associated ADP/ATP translocases in Rickettsia and mitochondria are not specifically related, evidently having arisen independently during the intracellular adaptation of parasite and organelle, after their divergence from a last common ancestor. In fact, many of the metabolic similarities between Rickettsia and mitochondria (for example, the absence of glycolytic enzymes) probably reflect convergent evolution rather than vertical inheritance [12,27,30].

Although differing in detail, both of these studies [34,35] come to similar general conclusions about the origin of the yeast mitochondrial proteome. In particular, the two studies - which both consist fundamentally of similarity searches - identify three categories of yeast mitochondrial proteins (Figure 1): ‘prokaryote-specific’ (50-60% of the total), ‘eukaryote-specific’ (20-30%) and ‘organism-specific’, or ‘unique’ (about 20%). Prokaryote-specific mitochondrial proteins are defined as those that have counterparts in prokaryotic genomes; eukaryote-specific mitochondrial proteins have counterparts in other eukaryotic genomes but not in prokaryotic genomes; and organism-specific mitochondrial proteins are ones so far unique to S. cerevisiae. In addition, both studies point out that this classification correlates with the known or inferred functions of the proteins in each category: prokaryote-specific mitochondrial proteins predominantly perform roles in biosynthesis, bioenergetics and protein synthesis, whereas eukaryote-specific mitochondrial proteins function mainly as membrane components and in regulation and transport.

Post a Comment

You must be logged in to post a comment.