Does mitochondrial DNA evolution in metazoa drive the origin of new mitochondrial proteins?

Abstract

Most eukaryotic cells contain mitochondria with a genome that evolved from their α-proteobacterial ancestor. In the course of eukaryotic evolution, the mitochondrial genome underwent a dramatic reduction in size, caused by the loss and translocation of genes. This required adjustments in mitochondrial gene expression mechanisms and resulted in a complex collaborative system of mitochondrially encoded transfer RNAs and ribosomal RNAs with nuclear encoded proteins to express the mitochondrial encoded oxidative phosphorylation (OXPHOS) proteins. In this review, we examine mitochondrial gene expression from an evolutionary point of view: to what extent can we correlate changes in the mitochondrial genome in the evolutionary lineage leading to human with the origin of new nuclear encoded proteins. We dated the evolutionary origin of mitochondrial proteins that interact with mitochondrial DNA or its RNA and/or protein products in a systematic manner and compared them with documented changes in the mitochondrial DNA. We find anecdotal but accumulating evidence that metazoan RNA-interacting proteins arose in conjunction with changes of the mitochondrial DNA. We find no substantial evidence for such compensatory evolution in new OXPHOS proteins, which appear to be constrained by the ability to form supercomplexes.

Composition and stage dynamics of mitochondrial complexes inPlasmodium falciparum

“…For the novel uncharacterized and apicomplexan-specific OXPHOS complex subunits, it is challenging to estimate biological significance or function. It is tempting to speculate that some of the new, transmembrane helix containing proteins are functional and structural replacements of the two missing subunits in CIV, however, as we have observed in the evolution of CI in Metazoa, evolutionary new subunits do not necessarily occupy the same location in the complex where subunits are missing (76). Nevertheless, the observed complexes allow us to draw some important conclusions and raise interesting questions.…”

“…An alternative explanation could be that the transfer of genes originally found on mtDNA to the nucleus necessitated amino acid changes to facilitate import into the mitochondrion, which in turn required incorporation of additional subunits to maintain the same functionality. Although this is a tempting hypothesis, no strong evidence for it has been obtained from the analysis of the evolution of the mitochondrial genome in conjunction with the mitochondrial proteome in other evolutionary lineages (76,80). Finally, there also could be a lack of energetic constraints that are afforded by the parasitic lifestyle, which may have allowed the passing on of such bulky complexes.…”

The complete mitochondrial genome of medicinal fungus Taiwanofungus camphoratus reveals gene rearrangements and intron dynamics of Polyporales

“…As the 'second genome' of eukaryotes, mitochondrial genome plays an important role in aging, death, disease occurrence and stress resistance of eukaryotes [54][55][56] . Mitochondrial genome organization, core protein coding genes, repetitive sequences, gene arrangement, the number and structure of tRNAs, and open reading frames provided rich genetic information for understanding the genitics and evolution of eukaryotes [57][58][59] . Mitochondrial genomes have been extensively studied in animals.…”

Recurrent erosion ofCOA1/MITRAC15demonstrates gene dispensability in oxidative phosphorylation

“…Despite the movement of most genes from the ancestral mitochondria to the nucleus in eukaryotes, a separate mitochondrial organelle is well conserved with scarce exceptions (Karnkowska et al, 2016; Sloan et al, 2018). Turnover in the content of mitochondrial protein complexes has mainly occurred before the emergence of eukaryotes with few gene gain/loss events reported in vertebrates (Adams and Palmer, 2003; Cardol, 2011; Gabaldón et al, 2005; Gabaldón and Huynen, 2007; Huynen et al, 2013; van Esveld and Huynen, 2018). However, lineage-specific gene loss from the mitochondria has occurred in nonbilaterian organisms (Lavrov and Pett, 2016), other metazoan lineages (Gissi et al, 2008), and plants (Depamphilis et al, 1997; Palmer et al, 2000).…”