Evolution of mitochondrial TAT translocases illustrates the loss of bacterial protein transport machines in mitochondria

Abstract

BackgroundBacteria and mitochondria contain translocases that function to transport proteins across or insert proteins into their inner and outer membranes. Extant mitochondria retain some bacterial-derived translocases but have lost others. While BamA and YidC were integrated into general mitochondrial protein transport pathways (as Sam50 and Oxa1), the inner membrane TAT translocase, which uniquely transports folded proteins across the membrane, was retained sporadically across the eukaryote tree.ResultsWe have identified mitochondrial TAT machinery in diverse eukaryotic lineages and define three different types of eukaryote-encoded TatABC-derived machineries (TatAC, TatBC and TatC-only). Here, we investigate TatAC and TatC-only machineries, which have not been studied previously. We show that mitochondria-encoded TatAC of the jakobid Andalucia godoyi represent the minimal functional pathway capable of substituting for the Escherichia coli TatABC complex and can transport at least one substrate. However, selected TatC-only machineries, from multiple eukaryotic lineages, were not capable of supporting the translocation of this substrate across the bacterial membrane. Despite the multiple losses of the TatC gene from the mitochondrial genome, the gene was never transferred to the cell nucleus. Although the major constraint preventing nuclear transfer of mitochondrial TatC is likely its high hydrophobicity, we show that in chloroplasts, such transfer of TatC was made possible due to modifications of the first transmembrane domain.ConclusionsAt its origin, mitochondria inherited three inner membrane translocases Sec, TAT and Oxa1 (YidC) from its bacterial ancestor. Our work shows for the first time that mitochondrial TAT has likely retained its unique function of transporting folded proteins at least in those few eukaryotes with TatA and TatC subunits encoded in the mitochondrial genome. However, mitochondria, in contrast to chloroplasts, abandoned the machinery multiple times in evolution. The overall lower hydrophobicity of the Oxa1 protein was likely the main reason why this translocase was nearly universally retained in mitochondrial biogenesis pathways.Electronic supplementary materialThe online version of this article (10.1186/s12915-018-0607-3) contains supplementary material, which is available to authorized users.

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 proteobacteria, the minimal active TAT system consists of three proteins, TatA, TatB, and TatC [168]. Orthologs of TatA and TatC, encoded by mtDNA, have a scattered distribution among eukaryotes, but whether these proteins constitute an active system in the organelle is not clear [169]. In plants, whose mitochondrial genomes encode only TatC, a TatB but apparently not TatA ortholog is encoded in the nuclear genome, and a functional TatB-TatC complex has been proposed in this case [170].…”

Mitochondrial Genome Sequence ofPhytophthora sansomeanaand Comparative Analysis ofPhytophthoraMitochondrial Genomes

“…The TatC protein is an essential component of the Tat system. In a previous study, TatC gene was identified in the mitochondrial genomes of oomycetes [42]. To determine the function of ymf16 gene, its predicted protein sequences from the 10…”

Peer Review #1 of "The inflated mitochondrial genomes of siphonous green algae reflect processes driving expansion of noncoding DNA and proliferation of introns (v0.1)"

“…It also encodes named protein-coding genes commonly found in green algae (Table 3, S3). This does include some genes that are less common in Chlorophyta mitochondrial genomes: nad10, which is absent from the mtDNA of sequenced land plants and many green algae (Mower et al, 2012), and tatC, a gene encoding a component of the inner membrane TAT translocase responsible for transporting folded proteins across the membrane in bacteria but whose function in mitochondria remains unclear (Carrie et al, 2016;Petrů et al, 2018).…”