Origin and Evolutionary Alteration of the Mitochondrial Import System in Eukaryotic Lineages

Abstract

Protein transport systems are fundamentally important for maintaining mitochondrial function. Nevertheless, mitochondrial protein translocases such as the kinetoplastid ATOM complex have recently been shown to vary in eukaryotic lineages. Various evolutionary hypotheses have been formulated to explain this diversity. To resolve any contradiction, estimating the primitive state and clarifying changes from that state are necessary. Here, we present more likely primitive models of mitochondrial translocases, specifically the translocase of the outer membrane (TOM) and translocase of the inner membrane (TIM) complexes, using scrutinized phylogenetic profiles. We then analyzed the translocases’ evolution in eukaryotic lineages. Based on those results, we propose a novel evolutionary scenario for diversification of the mitochondrial transport system. Our results indicate that presequence transport machinery was mostly established in the last eukaryotic common ancestor, and that primitive translocases already had a pathway for transporting presequence-containing proteins. Moreover, secondary changes including convergent and migrational gains of a presequence receptor in TOM and TIM complexes, respectively, likely resulted from constrained evolution. The nature of a targeting signal can constrain alteration to the protein transport complex.

The draft nuclear genome sequence and predicted mitochondrial proteome of Andalucia godoyi, a protist with the most gene-rich and bacteria-like mitochondrial genome

“…In fungi, the TIM22 complex comprises Tim22, the channel-forming protein; Tim54, a receptor-like protein; and Tim18, which like Tim22 is imbedded in the MIM. Of these, we detected only Tim22 in Andalucia, consistent with recent work [161] showing that Tim54 and Tim18 are fungal-specific components. As expected, Andalucia also lacks a homolog of the mammalianspecific Tim29 subunit [162].…”

“…Nevertheless, certain complexes do appear to be simpler in Andalucia (e.g., MICOS, TOM, TIM22; Fig. 6), suggesting either that some components have been secondarily lost or that further subunits were incorporated into these complexes in a lineage-specific fashion later in evolution (see, e.g., [149,161]). This apparent simplicity compared to animals, fungi, and land plants (primarily multicellular eukaryotes) is not unique to Andalucia, but applies to other protists, as well.…”

Targeting mitochondrial and cytosolic substrates of TRIT1 isopentenyltransferase: Specificity determinants and tRNA-i6A37 profiles

“…Mitochondrial protein import pathways have been functionally conserved in eukaryotes including mammals and yeasts [57,58]; S. cerevisiae, S. pombe, D. melanogaster and H. Sapiens share Tom20, five other TOM homologs, and twelve of the thirteen TIM (translocase of the inner mitochondrial membrane) system components [58]. Analysis of S. pombe mt-DNA by tRNAscan-SE predicts 25 mt-tRNAs (including 3 for Met), of which two, mt-tRNA Trp CCA and mt-tRNA Cys GCA contain A36-A37-A38.…”

Evidence supporting an antimicrobial origin of targeting peptides to endosymbiotic organelles

“…TPs are recognized by the main mitochondrial and chloroplast translocation pathways (Wiedemann and Pfanner 2017;Nakai 2018) and destroyed upon import into organelles (Neupert and Herrmann 2007;Chotewutmontri et al 2017). The emergence of such TP-based import, despite being a key innovation enabling endosymbiosis and eukaryotism, remains poorly understood (Fukasawa et al 2017;Reumann et al 2005;Nakai 2018).…”