Triplet-pore structure of a highly divergent TOM complex of hydrogenosomes in <i>Trichomonas vaginalis</i>

MAKKI, Abhijith, Petr RADA, Vojtech ZARSKY, Sami KEREICHE, Lubomir KOVACIK, Marian NOVOTNY, Tobias JORES, Doron RAPAPORT and Jan TACHEZY. Triplet-pore structure of a highly divergent TOM complex of hydrogenosomes in <i>Trichomonas vaginalis</i>. PLoS Biology. USA: PUBLIC LIBRARY SCIENCE, 2019, vol. 17, No 1, 32 pp. ISSN 1544-9173. Available from: https://dx.doi.org/10.1371/journal.pbio.3000098.

Basic information

• Original name: Triplet-pore structure of a highly divergent TOM complex of hydrogenosomes in <i>Trichomonas vaginalis</i>
• Authors: MAKKI, Abhijith, Petr RADA, Vojtech ZARSKY, Sami KEREICHE, Lubomir KOVACIK, Marian NOVOTNY, Tobias JORES, Doron RAPAPORT and Jan TACHEZY.
• Edition: PLoS Biology, USA, PUBLIC LIBRARY SCIENCE, 2019, 1544-9173.

Other information

• Original language: English
• Type of outcome: Article in a journal
• Field of Study: 10608 Biochemistry and molecular biology
• Country of publisher: United States of America
• Confidentiality degree: is not subject to a state or trade secret
• WWW: URL
• Impact factor: Impact factor: 7.076
• Organization unit: Central European Institute of Technology
• Doi: http://dx.doi.org/10.1371/journal.pbio.3000098
• UT WoS: 000457596000015
• Keywords in English: MITOCHONDRIAL IMPORT RECEPTOR; BETA-BARREL PROTEINS; CRYO-EM STRUCTUREOUTER-MEMBRANEWEB SERVERCORE COMPLEXEVOLUTIONSEQUENCEPROTEOMEGENOME
• Tags: CF CRYO
• Tags: International impact, Reviewed

Abstract

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 beta-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 beta-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.