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Triplet-Pore Structure of a Highly Divergent TOM Complex of Hydrogenosomes in Trichomonas Vaginalis

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Triplet-Pore Structure of a Highly Divergent TOM Complex of Hydrogenosomes in Trichomonas Vaginalis RESEARCH ARTICLE Triplet-pore structure of a highly divergent TOM complex of hydrogenosomes in Trichomonas vaginalis 1 1 1 2 2 Abhijith MakkiID , Petr RadaID , Vojtěch ZÏ aÂrsky , Sami KereïcheID , LubomõÂr KovaÂčikID , 3 4 4 1 Marian Novotny ID , Tobias JoresID , Doron Rapaport , Jan TachezyID * 1 Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Prague, Czech Republic, 2 Institute of Biology and Medical Genetics, First Faculty of Medicine, Charles University, Prague, Czech Republic, 3 Department of Cell Biology, Faculty of Science, Charles University, Prague, Czech Republic, a1111111111 4 Interfaculty Institute of Biochemistry, University of TuÈbingen, TuÈbingen, Germany a1111111111 a1111111111 * [email protected] a1111111111 a1111111111 Abstract Mitochondria originated from proteobacterial endosymbionts, and their transition to organ- elles was tightly linked to establishment of the protein import pathways. The initial import OPEN ACCESS of most proteins is mediated by the translocase of the outer membrane (TOM). Although Citation: Makki A, Rada P, ZÏaÂrsky V, Kereïche S, KovaÂčik L, Novotny M, et al. (2019) Triplet-pore TOM is common to all forms of mitochondria, an unexpected diversity of subunits between structure of a highly divergent TOM complex of eukaryotic lineages has been predicted. However, experimental knowledge is limited to a hydrogenosomes in Trichomonas vaginalis. PLoS few organisms, and so far, it remains unsettled whether the triplet-pore or the twin-pore Biol 17(1): e3000098. https://doi.org/10.1371/ structure is the generic form of TOM complex. Here, we analysed the TOM complex in journal.pbio.3000098 hydrogenosomes, a metabolically specialised anaerobic form of mitochondria found in the Academic Editor: Andre Schneider, Universitat excavate Trichomonas vaginalis. We demonstrate that the highly divergent β-barrel T. vagi- Bern, SWITZERLAND nalis TOM (TvTom)40-2 forms a translocation channel to conduct hydrogenosomal protein Received: October 24, 2018 import. TvTom40-2 is present in high molecular weight complexes, and their analysis Accepted: December 11, 2018 revealed the presence of four tail-anchored (TA) proteins. Two of them, Tom36 and Tom46, Published: January 4, 2019 with heat shock protein (Hsp)20 and tetratricopeptide repeat (TPR) domains, can bind Copyright: © 2019 Makki et al. This is an open hydrogenosomal preproteins and most likely function as receptors. A third subunit, Tom22- access article distributed under the terms of the like protein, has a short cis domain and a conserved Tom22 transmembrane segment but Creative Commons Attribution License, which lacks a trans domain. The fourth protein, hydrogenosomal outer membrane protein 19 permits unrestricted use, distribution, and (Homp19) has no known homology. Furthermore, our data indicate that TvTOM is associ- reproduction in any medium, provided the original author and source are credited. ated 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 Data Availability Statement: The mass spectrometry data are available via PRIDE an unconventional skull-like shape. Although TvTOM seems to lack Tom7, our phylogenetic repository under the project accession profiling predicted Tom7 in free-living excavates. Collectively, our results suggest that the PXD010850. triplet-pore TOM complex, composed of three conserved subunits, was present in the last Funding: This work was supported by the common eukaryotic ancestor (LECA), while receptors responsible for substrate binding programs KONTAKT II (LH15254), NPU II evolved independently in different eukaryotic lineages. (LQ1604) provided by the Ministry of Education, Youth and Sport (MEYS), CePaViP (CZ.02.1.01/ 0.0/0.0/16_019/0000759) (to JT) supported by ERD Funds, Charles University projects - GAUK 268715 and GAUK 250937 (to AM), UNCE 204022 PLOS Biology | https://doi.org/10.1371/journal.pbio.3000098 January 4, 2019 1 / 32 Divergent TOM complex of hydrogenosomes in Trichomonas vaginalis (to SK), and GAČR Centre of Excellence project P302/12/G157 (to LK). We thank Karel Harant and Author summary Pavel Talacko from the Laboratory of Mass Spectrometry, BIOCEV. We acknowledge the core Mitochondria carry out many vital functions in the eukaryotic cells, from energy metabo- facility Cryo-Electron Microscopy and lism to programmed cell death. These organelles descended from bacterial endosymbi- Tomography, CEITEC supported by the CIISB onts, and during their evolution, the cell established a mechanism to transport nuclear- (LM2015043 funded by MEYS CR), and the IMCF, encoded proteins into mitochondria. Embedded in the mitochondrial outer membrane is BIOCEV, supported by the Czech-BioImaging RI a molecular machine, known as the translocase of the outer membrane (TOM) complex, project LM2015062. The funders had no role in study design, data collection and analysis, decision that plays a key role in protein import and biogenesis of the organelle. Here, we provide to publish, or preparation of the manuscript. evidence that the TOM complex of hydrogenosomes, a metabolically specialised anaerobic form of mitochondria in , is composed of highly divergent core sub- Competing interests: The authors have declared Trichomonas vaginalis that no competing interests exist. units and lineage-specific peripheral subunits. Despite the evolutionary distance, the T. vaginalis TOM (TvTOM) complex has a conserved triplet-pore structure but with a Abbreviations: SCS, -subunit of succinyl CoA α α unique skull-like shape suggesting that the TOM in the early mitochondrion could have synthetase; 2D, two-dimensional; 3D, three- dimensional; ATOM, archaic translocase of the formed three pores. Our results contribute to a better understanding of the evolution and outer membrane; BN-PAGE, blue native PAGE; adaptation of protein import machinery in anaerobic forms of mitochondria. CLANS, cluster analysis of sequences; CoA, coenzyme A; COG, clusters of orthologous groups; coIP, co-immunoprecipitation; Cryo-EM, Cryo electron microscopy; CTF, Contrast Transfer Introduction Function; cytME, cytoplasmic malic enzyme; DHFR, Mitochondria originated from proteobacterial endosymbionts [1], and over time, massive dihydrofolate reductase; DIC, differential interference contrast; Dox, doxycycline; ERAD, endosymbiotic gene transfer to the host nucleus or gene deletion forged the development of a endoplasmic reticulum-associated protein mechanism for retargeting of nuclear-encoded proteins to the evolving organelle [2]. To cross degradation; FASP, filter-aided sample preparation; the double membrane of the mitochondrion, the proteins had to pass through the translocase Fdx, ferredoxin; Fis1, mitochondrial fission 1; HA, of the outer (TOM) and inner (TIM) membranes. It has been inferred that most modules of human influenza hemagglutinin; HMM, hidden the import machinery were created de novo and the ancient TOM complex comprised at least Markov model; Hmp, hydrogenosomal membrane protein; Homp, hydrogenosomal outer membrane three components, the β-barrel translocation channel-forming Tom40 and two tail-anchored protein; Hsp, heat shock protein; IMS, (TA) proteins, Tom22 and Tom7 [3,4]. intermembrane space; IPTG, Isopropyl β-D-1- The TOM complex in yeast consists of Tom40 and six α-helical proteins: two that are thiogalactopyranoside; ITS, internal-targeting anchored to the outer mitochondrial membrane (OMM) by an N-terminal transmembrane sequence; LECA, last common eukaryotic ancestor; domain (TMD; Tom20 and Tom70) and four that are anchored by a C-terminal TMD LFQ-MS, label-free quantitative mass (Tom22, Tom5, Tom6, and Tom7). Tom20 and Tom70, both carrying tetratricopeptide repeat spectrometry; MAFFT, multiple sequence alignment based on fast Fourier transform; MS, (TPR) domains, serve as primary receptors recognising proteins with N-terminal targeting mass spectrometry; NCBI, National Center for sequence (NTS) and internal-targeting sequences (ITSs), respectively [5,6]. A prominent fea- Biotechnology Information; Ni-NTA, Ni- ture of the TOM complex is the variation in receptors across different eukaryotic lineages. A nitrilotriacetic acid; NTS, N-terminal targeting signal-anchored Tom20 is present in animals and fungi, whereas plant Tom20 evolved inde- sequence; OD, optical density; OMM, outer pendently with a C-terminal anchor [7]. Lineage-specific Tom20 and Tom60 without any mitochondrial membrane; PDB, Protein Data Bank; Pfam, Protein families; SAM, sorting and assembly TMD are present in amoebozoans [8,9]. Tom20 and Tom70 are essentially absent in the machinery; SAR, Stramenopiles, Alveolata and eukaryotic supergroup Excavata [10±12]. In the excavate Trypanosoma brucei, the TOM com- Rhizaria; SD-Leu, synthetic drop-out medium plex (named the archaic translocase of the outer membrane [ATOM]) has only two ortholo- without leucine; SDS-PAGE, sodium dodecyl gues, a highly divergent Tom40 (ATOM40) and a Tom22-like protein (ATOM14) [11,13]. sulphate-PAGE; STED, Stimulated Emission Instead of Tom70 and Tom20, two unique receptors were identified, a TA protein ATOM69 Depletion; TA, tail-anchored; TCA, tricarboxylic and a signal-anchored ATOM46 [11]. acid; TEM, transmission electron microscopy; TIM, translocase of the inner membrane; TMD, Structural studies of the contemporary TOM complex are exclusively based on fungi, Sac- transmembrane domain; TMHMM, charomyces cerevisiae and Neurospora crassa
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