Triplet-pore structure of a highly divergent TOM complex of hydrogenosomes in Trichomonas vaginalis.


Journal

PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755

Informations de publication

Date de publication:
01 2019
Historique:
received: 24 10 2018
accepted: 11 12 2018
revised: 16 01 2019
pubmed: 5 1 2019
medline: 5 11 2019
entrez: 5 1 2019
Statut: epublish

Résumé

Mitochondria originated from proteobacterial endosymbionts, and their transition to organelles was tightly linked to establishment of the protein import pathways. The initial import of most proteins is mediated by the translocase of the outer membrane (TOM). Although TOM is common to all forms of mitochondria, an unexpected diversity of subunits between eukaryotic lineages has been predicted. However, experimental knowledge is limited to a few organisms, and so far, it remains unsettled whether the triplet-pore or the twin-pore structure is the generic form of TOM complex. Here, we analysed the TOM complex in hydrogenosomes, a metabolically specialised anaerobic form of mitochondria found in the excavate Trichomonas vaginalis. We demonstrate that the highly divergent β-barrel T. vaginalis TOM (TvTom)40-2 forms a translocation channel to conduct hydrogenosomal protein import. TvTom40-2 is present in high molecular weight complexes, and their analysis revealed the presence of four tail-anchored (TA) proteins. Two of them, Tom36 and Tom46, with heat shock protein (Hsp)20 and tetratricopeptide repeat (TPR) domains, can bind hydrogenosomal preproteins and most likely function as receptors. A third subunit, Tom22-like protein, has a short cis domain and a conserved Tom22 transmembrane segment but lacks a trans domain. The fourth protein, hydrogenosomal outer membrane protein 19 (Homp19) has no known homology. Furthermore, our data indicate that TvTOM is associated with sorting and assembly machinery (Sam)50 that is involved in β-barrel assembly. Visualisation of TvTOM by electron microscopy revealed that it forms three pores and has an unconventional skull-like shape. Although TvTOM seems to lack Tom7, our phylogenetic profiling predicted Tom7 in free-living excavates. Collectively, our results suggest that the triplet-pore TOM complex, composed of three conserved subunits, was present in the last common eukaryotic ancestor (LECA), while receptors responsible for substrate binding evolved independently in different eukaryotic lineages.

Identifiants

pubmed: 30608924
doi: 10.1371/journal.pbio.3000098
pii: PBIOLOGY-D-18-01032
pmc: PMC6334971
doi:

Substances chimiques

Carrier Proteins 0
Membrane Proteins 0
Membrane Transport Proteins 0
Mitochondrial Membrane Transport Proteins 0
Mitochondrial Precursor Protein Import Complex Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e3000098

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Abhijith Makki (A)

Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Prague, Czech Republic.

Petr Rada (P)

Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Prague, Czech Republic.

Vojtěch Žárský (V)

Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Prague, Czech Republic.

Sami Kereïche (S)

Institute of Biology and Medical Genetics, First Faculty of Medicine, Charles University, Prague, Czech Republic.

Lubomír Kováčik (L)

Institute of Biology and Medical Genetics, First Faculty of Medicine, Charles University, Prague, Czech Republic.

Marian Novotný (M)

Department of Cell Biology, Faculty of Science, Charles University, Prague, Czech Republic.

Tobias Jores (T)

Interfaculty Institute of Biochemistry, University of Tübingen, Tübingen, Germany.

Doron Rapaport (D)

Interfaculty Institute of Biochemistry, University of Tübingen, Tübingen, Germany.

Jan Tachezy (J)

Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Prague, Czech Republic.

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