Abstract
BackgroundDuring the generation and evolution of the eukaryotic cell, a proteobacterial endosymbiont was re-fashioned into the mitochondrion, an organelle that appears to have been present in the ancestor of all present-day eukaryotes. Mitochondria harbor proteomes derived from coding information located both inside and outside the organelle, and the rate-limiting step toward the formation of eukaryotic cells may have been development of an import apparatus allowing protein entry to mitochondria. Currently, a widely conserved translocon allows proteins to pass from the cytosol into mitochondria, but how proteins encoded outside of mitochondria were first directed to these organelles at the dawn of eukaryogenesis is not clear. Because several proteins targeted by a carboxyl-terminal tail anchor (TA) appear to have the ability to insert spontaneously into the mitochondrial outer membrane (OM), it is possible that self-inserting, tail-anchored polypeptides obtained from bacteria might have formed the first gate allowing proteins to access mitochondria from the cytosol.ResultsHere, we tested whether bacterial TAs are capable of targeting to mitochondria. In a survey of proteins encoded by the proteobacterium Escherichia coli, predicted TA sequences were directed to specific subcellular locations within the yeast Saccharomyces cerevisiae. Importantly, TAs obtained from DUF883 family members ElaB and YqjD were abundantly localized to and inserted at the mitochondrial OM.ConclusionsOur results support the notion that eukaryotic cells are able to utilize membrane-targeting signals present in bacterial proteins obtained by lateral gene transfer, and our findings make plausible a model in which mitochondrial protein translocation was first driven by tail-anchored proteins.ReviewersThis article was reviewed by Michael Ryan and Thomas Simmen.
Highlights
During the generation and evolution of the eukaryotic cell, a proteobacterial endosymbiont was re-fashioned into the mitochondrion, an organelle that appears to have been present in the ancestor of all present-day eukaryotes
We focused our attention upon a single aspect of this hypothesis: can tail anchor (TA) obtained from bacterial proteins be inserted into the mitochondrial outer membrane (OM) when expressed within a eukaryotic cell? our results demonstrate insertion and function at the mitochondrial OM for predicted TAs encoded by the proteobacterium E. coli, and we describe the relevance of our findings to the concept of lateral gene transfer during eukaryogenesis
Bacterial tail anchors can localize to mitochondria To test whether predicted bacterial TAs might have the capacity to be inserted at the mitochondrial OM, we identified 12 E. coli proteins predicted to harbor a solitary α-helical transmembrane (TM) domain at the polypeptide carboxyl-terminus (Additional file 1: Figure S1), fused mCherry to the amino-terminus of these TAs and examined their location in S. cerevisiae cells by fluorescence microscopy. mCherry-ElaB(TA) (Fig. 1a) and mCherry-YqjD(TA) (Fig. 1b) were readily detectable at mitochondria, as reported by co-localization with superfolder GFP [18] fused to the TA of the S. cerevisiae Fis1 polypeptide, a protein playing a role in yeast mitochondrial division
Summary
During the generation and evolution of the eukaryotic cell, a proteobacterial endosymbiont was re-fashioned into the mitochondrion, an organelle that appears to have been present in the ancestor of all present-day eukaryotes. Because several proteins targeted by a carboxyl-terminal tail anchor (TA) appear to have the ability to insert spontaneously into the mitochondrial outer membrane (OM), it is possible that self-inserting, tail-anchored polypeptides obtained from bacteria might have formed the first gate allowing proteins to access mitochondria from the cytosol. Current evidence suggests that the self-insertion of tail-anchored proteins at the mitochondrial OM is possible [13,14,15], and some tail-anchored pro-apoptotic proteins appear to have the ability to generate membrane pores at Lutfullahoğlu-Bal et al Biology Direct (2017) 12:16 mitochondria [16, 17], making tenable such a scenario for the evolution of mitochondrial protein import. At the inception of mitochondria, such tail-anchored proteins would likely have been derived from prokaryotes, if mitochondria were required for the generation of the stereotypical compartmentalized structure of eukaryotes
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