Giardia intestinalis mitosomes undergo synchronized fission but not fusion and are constitutively associated with the endoplasmic reticulum

. 2017 Apr 03 ; 15 (1) : 27. [epub] 20170403

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28372543
Odkazy

PubMed 28372543
PubMed Central PMC5377515
DOI 10.1186/s12915-017-0361-y
PII: 10.1186/s12915-017-0361-y
Knihovny.cz E-zdroje

BACKGROUND: Mitochondria of opisthokonts undergo permanent fission and fusion throughout the cell cycle. Here, we investigated the dynamics of the mitosomes, the simplest forms of mitochondria, in the anaerobic protist parasite Giardia intestinalis, a member of the Excavata supergroup of eukaryotes. The mitosomes have abandoned typical mitochondrial traits such as the mitochondrial genome and aerobic respiration and their single role known to date is the formation of iron-sulfur clusters. RESULTS: In live experiments, no fusion events were observed between the mitosomes in G. intestinalis. Moreover, the organelles were highly prone to becoming heterogeneous. This suggests that fusion is either much less frequent or even absent in mitosome dynamics. Unlike in mitochondria, division of the mitosomes was absolutely synchronized and limited to mitosis. The association of the nuclear and the mitosomal division persisted during the encystation of the parasite. During the segregation of the divided mitosomes, the subset of the organelles between two G. intestinalis nuclei had a prominent role. Surprisingly, the sole dynamin-related protein of the parasite seemed not to be involved in mitosomal division. However, throughout the cell cycle, mitosomes associated with the endoplasmic reticulum (ER), although none of the known ER-tethering complexes was present. Instead, the ER-mitosome interface was occupied by the lipid metabolism enzyme long-chain acyl-CoA synthetase 4. CONCLUSIONS: This study provides the first report on the dynamics of mitosomes. We show that together with the loss of metabolic complexity of mitochondria, mitosomes of G. intestinalis have uniquely streamlined their dynamics by harmonizing their division with mitosis. We propose that this might be a strategy of G. intestinalis to maintain a stable number of organelles during cell propagation. The lack of mitosomal fusion may also be related to the secondary reduction of the organelles. However, as there are currently no reports on mitochondrial fusion in the whole Excavata supergroup, it is possible that the absence of mitochondrial fusion is an ancestral trait common to all excavates.

Zobrazit více v PubMed

Labbé K, Murley A, Nunnari J. Determinants and functions of mitochondrial behavior. Annu Rev Cell Dev Biol. 2014;30:357–91. doi: 10.1146/annurev-cellbio-101011-155756. PubMed DOI

Mishra P, Chan DC. Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol. 2014;15:634–46. doi: 10.1038/nrm3877. PubMed DOI PMC

Bleazard W, McCaffery JM, King EJ, Bale S, Mozdy A, Tieu Q, Nunnari J, Shaw JM. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol. 1999;1:298–304. doi: 10.1038/13014. PubMed DOI PMC

Mozdy AD, McCaffery JM, Shaw JM. Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p. J Cell Biol. 2000;151:367–80. doi: 10.1083/jcb.151.2.367. PubMed DOI PMC

Otera H, Wang C, Cleland MM, Setoguchi K, Yokota S, Youle RJ, Mihara K. Mff is an essential factor for mitochondrial recruitment of Drp1 during mitochondrial fission in mammalian cells. J Cell Biol. 2010;191:1141–58. doi: 10.1083/jcb.201007152. PubMed DOI PMC

Hales KG, Fuller MT. Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell. 1997;90:121–9. doi: 10.1016/S0092-8674(00)80319-0. PubMed DOI

Wong ED, Wagner JA, Gorsich SW, McCaffery JM, Shaw JM, Nunnari J. The dynamin-related GTPase, Mgm1p, is an intermembrane space protein required for maintenance of fusion competent mitochondria. J Cell Biol. 2000;151:341–52. doi: 10.1083/jcb.151.2.341. PubMed DOI PMC

Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK. ER tubules mark sites of mitochondrial division. Science. 2011;334:358–62. doi: 10.1126/science.1207385. PubMed DOI PMC

Murley A, Lackner LL, Osman C, West M, Voeltz GK, Walter P, Nunnari J. ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. Elife. 2013;2:e00422. doi: 10.7554/eLife.00422. PubMed DOI PMC

Rowland AA, Voeltz GK. Endoplasmic reticulum–mitochondria contacts: function of the junction. Nat Rev Mol Cell Biol. 2012;13:607–25. doi: 10.1038/nrm3440. PubMed DOI PMC

Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, Weissman JS, Walter P. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science. 2009;325:477–81. doi: 10.1126/science.1175088. PubMed DOI PMC

AhYoung AP, Jiang J, Zhang J, Khoi Dang X, Loo JA, Zhou ZH, Egea PF. Conserved SMP domains of the ERMES complex bind phospholipids and mediate tether assembly. Proc Natl Acad Sci U S A. 2015;112:E3179–88. doi: 10.1073/pnas.1422363112. PubMed DOI PMC

Murley A, Sarsam RD, Toulmay A, Yamada J, Prinz WA, Nunnari J. Ltc1 is an ER-localized sterol transporter and a component of ER-mitochondria and ER-vacuole contacts. J Cell Biol. 2015;209:539–48. doi: 10.1083/jcb.201502033. PubMed DOI PMC

Elbaz-Alon Y, Eisenberg-Bord M, Shinder V, Stiller SB, Shimoni E, Wiedemann N, Geiger T, Schuldiner M. Lam6 Regulates the Extent of Contacts between Organelles. Cell Rep. 2015;12:7–14. doi: 10.1016/j.celrep.2015.06.022. PubMed DOI PMC

de Brito OM, Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature. 2008;456:605–10. doi: 10.1038/nature07534. PubMed DOI

Filadi R, Greotti E, Turacchio G, Luini A, Pozzan T, Pizzo P. Mitofusin 2 ablation increases endoplasmic reticulum–mitochondria coupling. Proc Natl Acad Sci. 2015;112:E2174–81. doi: 10.1073/pnas.1504880112. PubMed DOI PMC

Adams DW, Errington J. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol. 2009;7:642–53. doi: 10.1038/nrmicro2198. PubMed DOI

Beech PL, Nheu T, Schultz T, Herbert S, Lithgow T, Gilson PR, McFadden GI. Mitochondrial FtsZ in a chromophyte alga. Science. 2000;287:1276–9. doi: 10.1126/science.287.5456.1276. PubMed DOI

Leger MM, Petrů M, Žárský V, Eme L, Vlček Č, Harding T, Lang BF, Eliáš M, Doležal P, Roger AJ. An ancestral bacterial division system is widespread in eukaryotic mitochondria. Proc Natl Acad Sci U S A. 2015;112:10239–46. doi: 10.1073/pnas.1421392112. PubMed DOI PMC

Chanez A-L, Hehl AB, Engstler M, Schneider A. Ablation of the single dynamin of T. brucei blocks mitochondrial fission and endocytosis and leads to a precise cytokinesis arrest. J Cell Sci. 2006;119:2968–74. doi: 10.1242/jcs.03023. PubMed DOI

Morgan GW, Goulding D, Field MC. The single dynamin-like protein of Trypanosoma brucei regulates mitochondrial division and is not required for endocytosis. J Biol Chem. 2004;279:10692–701. doi: 10.1074/jbc.M312178200. PubMed DOI

Wexler-Cohen Y, Stevens GC, Barnoy E, van der Bliek AM, Johnson PJ. A dynamin-related protein contributes to Trichomonas vaginalis hydrogenosomal fission. FASEB J. 2014;28:1113–21. doi: 10.1096/fj.13-235473. PubMed DOI PMC

Niemann M, Wiese S, Mani J, Chanfon A, Jackson C, Meisinger C, Warscheid B, Schneider A. Mitochondrial outer membrane proteome of Trypanosoma brucei reveals novel factors required to maintain mitochondrial morphology. Mol Cell Proteomics. 2013;12:515–28. doi: 10.1074/mcp.M112.023093. PubMed DOI PMC

Schneider RE, Brown MT, Shiflett AM, Dyall SD, Hayes RD, Xie Y, Loo JA, Johnson PJ. The Trichomonas vaginalis hydrogenosome proteome is highly reduced relative to mitochondria, yet complex compared with mitosomes. Int J Parasitol. 2011;41:1421–34. doi: 10.1016/j.ijpara.2011.10.001. PubMed DOI PMC

Makiuchi T, Nozaki T. Highly divergent mitochondrion-related organelles in anaerobic parasitic protozoa. Biochimie. 2014;100:3–17. doi: 10.1016/j.biochi.2013.11.018. PubMed DOI

O’Malley MA, Wideman JG, Ruiz-Trillo I. Losing complexity: the role of simplification in macroevolution. Trends Ecol Evol. 2016;31(8):608–21. doi: 10.1016/j.tree.2016.04.004. PubMed DOI

Jedelský PL, Doležal P, Rada P, Pyrih J, Smíd O, Hrdý I, Sedinová M, Marcinčiková M, Voleman L, Perry AJ, Beltrán NC, Lithgow T, Tachezy J. The minimal proteome in the reduced mitochondrion of the parasitic protist Giardia intestinalis. PLoS One. 2011;6:e17285. doi: 10.1371/journal.pone.0017285. PubMed DOI PMC

Mi-ichi F, Abu Yousuf M, Nakada-Tsukui K, Nozaki T. Mitosomes in Entamoeba histolytica contain a sulfate activation pathway. Proc Natl Acad Sci U S A. 2009;106:21731–6. doi: 10.1073/pnas.0907106106. PubMed DOI PMC

Tovar J, León-Avila G, Sánchez LB, Sutak R, Tachezy J, van der Giezen M, Hernández M, Müller M, Lucocq JM. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature. 2003;426:172–6. doi: 10.1038/nature01945. PubMed DOI

Ankarklev J, Jerlström-Hultqvist J, Ringqvist E, Troell K, Svärd SG. Behind the smile: cell biology and disease mechanisms of Giardia species. Nat Rev Microbiol. 2010;8:413–22. PubMed

Martincová E, Voleman L, Najdrová V, De Napoli M, Eshar S, Gualdron M, Hopp CS, Sanin DE, Tembo DL, Van Tyne D, Walker D, Marcinčiková M, Tachezy J, Doležal P. Live imaging of mitosomes and hydrogenosomes by HaloTag technology. PLoS One. 2012;7:e36314. doi: 10.1371/journal.pone.0036314. PubMed DOI PMC

Regoes A, Zourmpanou D, León-Avila G, van der Giezen M, Tovar J, Hehl AB. Protein import, replication, and inheritance of a vestigial mitochondrion. J Biol Chem. 2005;280:30557–63. doi: 10.1074/jbc.M500787200. PubMed DOI

Martincová E, Voleman L, Pyrih J, Žárský V, Vondráčková P, Kolísko M, Tachezy J, Doležal P. Probing the biology of Giardia intestinalis mitosomes using in vivo enzymatic tagging. Mol Cell Biol. 2015;35:2864–74. doi: 10.1128/MCB.00448-15. PubMed DOI PMC

Brown DM, Upcroft JA, Edwards MR, Upcroft P. Anaerobic bacterial metabolism in the ancient eukaryote Giardia duodenalis. Int J Parasitol. 1998;28:149–64. doi: 10.1016/S0020-7519(97)00172-0. PubMed DOI

Sutak R, Dolezal P, Fiumera HL, Hrdy I, Dancis A, Delgadillo-Correa M, Johnson PJ, Müller M, Tachezy J. Mitochondrial-type assembly of FeS centers in the hydrogenosomes of the amitochondriate eukaryote Trichomonas vaginalis. Proc Natl Acad Sci U S A. 2004;101:10368–73. doi: 10.1073/pnas.0401319101. PubMed DOI PMC

Tejman-Yarden N, Eckmann L. New approaches to the treatment of giardiasis. Curr Opin Infect Dis. 2011;24:451–6. doi: 10.1097/QCO.0b013e32834ad401. PubMed DOI

Liu SM, Brown DM, O’Donoghue P, Upcroft P, Upcroft JA. Ferredoxin involvement in metronidazole resistance of Giardia duodenalis. Mol Biochem Parasitol. 2000;108:137–40. doi: 10.1016/S0166-6851(00)00194-8. PubMed DOI

Land KM, Clemens DL, Johnson PJ. Loss of multiple hydrogenosomal proteins associated with organelle metabolism and high-level drug resistance in trichomonads. Exp Parasitol. 2001;97:102–10. doi: 10.1006/expr.2001.4587. PubMed DOI

Benchimol M. The hydrogenosome. In: Hohmann-Marriott MF, editor. The structural basis of biological energy generation. Dordrecht: Springer Netherlands; 2014. pp. 419–33.

Chen H, Chomyn A, Chan DC. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J Biol Chem. 2005;280:26185–92. doi: 10.1074/jbc.M503062200. PubMed DOI

Hermann GJ, Thatcher JW, Mills JP, Hales KG, Fuller MT, Nunnari J, Shaw JM. Mitochondrial fusion in yeast requires the transmembrane GTPase Fzo1p. J Cell Biol. 1998;143:359–73. doi: 10.1083/jcb.143.2.359. PubMed DOI PMC

Gustafsson MGL, Shao L, Carlton PM, Wang CJR, Golubovskaya IN, Cande WZ, Agard DA, Sedat JW. Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys J. 2008;94:4957–70. doi: 10.1529/biophysj.107.120345. PubMed DOI PMC

Nohynková E, Tumová P, Kulda J. Cell division of Giardia intestinalis: flagellar developmental cycle involves transformation and exchange of flagella between mastigonts of a diplomonad cell. Eukaryot Cell. 2006;5:753–61. doi: 10.1128/EC.5.4.753-761.2006. PubMed DOI PMC

Striepen B, Crawford MJ, Shaw MK, Tilney LG, Seeber F, Roos DS. The plastid of Toxoplasma gondii is divided by association with the centrosomes. J Cell Biol. 2000;151:1423–34. doi: 10.1083/jcb.151.7.1423. PubMed DOI PMC

Nishida K, Takahara M, Miyagishima S, Kuroiwa H, Matsuzaki M, Kuroiwa T. Dynamic recruitment of dynamin for final mitochondrial severance in a primitive red alga. Proc Natl Acad Sci U S A. 2003;100:2146–51. doi: 10.1073/pnas.0436886100. PubMed DOI PMC

Pucadyil TJ, Schmid SL. Real-time visualization of dynamin-catalyzed membrane fission and vesicle release. Cell. 2008;135:1263–75. doi: 10.1016/j.cell.2008.11.020. PubMed DOI PMC

Hehl AB, Regos A, Schraner E, Schneider A. Bax function in the absence of mitochondria in the primitive protozoan Giardia lamblia. PLoS One. 2007;2:e488. doi: 10.1371/journal.pone.0000488. PubMed DOI PMC

Sagolla MS, Dawson SC, Mancuso JJ, Cande WZ. Three-dimensional analysis of mitosis and cytokinesis in the binucleate parasite Giardia intestinalis. J Cell Sci. 2006;119:4889–900. doi: 10.1242/jcs.03276. PubMed DOI

Meng TC, Aley SB, Svard SG, Smith MW, Huang B, Kim J, Gillin FD. Immunolocalization and sequence of caltractin/centrin from the early branching eukaryote Giardia lamblia. Mol Biochem Parasitol. 1996;79:103–8. doi: 10.1016/0166-6851(96)02636-9. PubMed DOI

Elias EV, Quiroga R, Gottig N, Nakanishi H, Nash TE, Neiman A, Lujan HD. Characterization of SNAREs determines the absence of a typical Golgi apparatus in the ancient eukaryote Giardia lamblia. J Biol Chem. 2008;283:35996–6010. doi: 10.1074/jbc.M806545200. PubMed DOI PMC

Hehl AB, Marti M. Secretory protein trafficking in Giardia intestinalis. Mol Microbiol. 2004;53:19–28. doi: 10.1111/j.1365-2958.2004.04115.x. PubMed DOI

Bernander R, Palm JE, Svärd SG. Genome ploidy in different stages of the Giardia lamblia life cycle. Cell Microbiol. 2001;3:55–62. doi: 10.1046/j.1462-5822.2001.00094.x. PubMed DOI

Labrousse AM, Zappaterra MD, Rube DA, van der Bliek AM. C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol Cell. 1999;4:815–26. doi: 10.1016/S1097-2765(00)80391-3. PubMed DOI

Korobova F, Ramabhadran V, Higgs HN. An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science. 2013;339:464–7. doi: 10.1126/science.1228360. PubMed DOI PMC

Gaechter V, Schraner E, Wild P, Hehl AB. The single dynamin family protein in the primitive protozoan Giardia lamblia is essential for stage conversion and endocytic transport. Traffic. 2008;9:57–71. doi: 10.1111/j.1600-0854.2007.00657.x. PubMed DOI

Paredez AR, Assaf ZJ, Sept D, Timofejeva L, Dawson SC, Wang C-JR, Cande WZ. An actin cytoskeleton with evolutionarily conserved functions in the absence of canonical actin-binding proteins. Proc Natl Acad Sci U S A. 2011;108:6151–6. doi: 10.1073/pnas.1018593108. PubMed DOI PMC

Zumthor JP, Cernikova L, Rout S, Kaech A, Faso C, Hehl AB. Static clathrin assemblies at the peripheral vacuole-plasma membrane interface of the parasitic protozoan Giardia lamblia. PLoS Pathog. 2016;12:e1005756. doi: 10.1371/journal.ppat.1005756. PubMed DOI PMC

Simpson AGB. Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota) Int J Syst Evol Microbiol. 2003;53:1759–77. doi: 10.1099/ijs.0.02578-0. PubMed DOI

Lahiri S, Chao JT, Tavassoli S, Wong AKO, Choudhary V, Young BP, Loewen CJR, Prinz WA. A conserved endoplasmic reticulum membrane protein complex (EMC) facilitates phospholipid transfer from the ER to mitochondria. PLoS Biol. 2014;12:e1001969. doi: 10.1371/journal.pbio.1001969. PubMed DOI PMC

Wideman JG, Gawryluk RMR, Gray MW, Dacks JB. The ancient and widespread nature of the ER-mitochondria encounter structure. Mol Biol Evol. 2013;30:2044–9. doi: 10.1093/molbev/mst120. PubMed DOI

Wideman JG. The ubiquitous and ancient ER membrane protein complex (EMC): tether or not? F1000Res. 2015;4:624. PubMed PMC

Vance JE. MAM (mitochondria-associated membranes) in mammalian cells: lipids and beyond. Biochim Biophys Acta. 2014;1841:595–609. doi: 10.1016/j.bbalip.2013.11.014. PubMed DOI

Yichoy M, Duarte TT, Chatterjee ADE, Mendez TL. Lipid metabolism in Giardia : a post-genomic perspective. 2011. pp. 267–78. PubMed PMC

Embley TM, Martin W. Eukaryotic evolution, changes and challenges. Nature. 2006;440:623–30. doi: 10.1038/nature04546. PubMed DOI

Dolezal P, Smíd O, Rada P, Zubácová Z, Bursać D, Suták R, Nebesárová J, Lithgow T, Tachezy J. Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc Natl Acad Sci U S A. 2005;102:10924–9. doi: 10.1073/pnas.0500349102. PubMed DOI PMC

Robinson DR, Gull K. Basal body movements as a mechanism for mitochondrial genome segregation in the trypanosome cell cycle. Nature. 1991;352:731–3. doi: 10.1038/352731a0. PubMed DOI

Nishi M, Hu K, Murray JM, Roos DS. Organellar dynamics during the cell cycle of Toxoplasma gondii. J Cell Sci. 2008;121:1559–68. doi: 10.1242/jcs.021089. PubMed DOI PMC

Gray MW, Lang BF, Burger G. Mitochondria of protists. Annu Rev Genet. 2004;38:477–524. doi: 10.1146/annurev.genet.37.110801.142526. PubMed DOI

Kuroiwa T, Nishida K, Yoshida Y, Fujiwara T, Mori T, Kuroiwa H, Misumi O. Structure, function and evolution of the mitochondrial division apparatus. Biochim Biophys Acta. 2006;1763:510–21. doi: 10.1016/j.bbamcr.2006.03.007. PubMed DOI

Rout S, Zumthor JP, Schraner EM, Faso C, Hehl AB. An interactome-centered protein discovery approach reveals novel components involved in mitosome function and homeostasis in Giardia lamblia. Kumar K, editor. PLoS Pathog. 2016;12:e1006036. doi: 10.1371/journal.ppat.1006036. PubMed DOI PMC

Beltrán NC, Horváthová L, Jedelský PL, Šedinová M, Rada P, Marcinčiková M, Hrdý I, Tachezy J. Iron-induced changes in the proteome of Trichomonas vaginalis hydrogenosomes. PLoS One. 2013;8:e65148. doi: 10.1371/journal.pone.0065148. PubMed DOI PMC

Gao H, Sage TL, Osteryoung KW. FZL, an FZO-like protein in plants, is a determinant of thylakoid and chloroplast morphology. Proc Natl Acad Sci U S A. 2006;103:6759–64. doi: 10.1073/pnas.0507287103. PubMed DOI PMC

Yu DC, Wang AL, Wang CC. Stable coexpression of a drug-resistance gene and a heterologous gene in an ancient parasitic protozoan Giardia lamblia. Mol Biochem Parasitol. 1996;83:81–91. doi: 10.1016/S0166-6851(96)02752-1. PubMed DOI

McCaffery JM, Gillin FD. Giardia lamblia: ultrastructural basis of protein transport during growth and encystation. Exp Parasitol. 1994;79:220–35. doi: 10.1006/expr.1994.1086. PubMed DOI

Vanácová S, Rasoloson D, Rázga J, Hrdý I, Kulda J, Tachezy J. Iron-induced changes in pyruvate metabolism of Tritrichomonas foetus and involvement of iron in expression of hydrogenosomal proteins. Microbiology. 2001;147:53–62. doi: 10.1099/00221287-147-1-53. PubMed DOI

Wideman JG, Muñoz-Gómez SA. The evolution of ERMIONE in mitochondrial biogenesis and lipid homeostasis: an evolutionary view from comparative cell biology. Biochim Biophys Acta. 2016;1861(8 Pt B):900–12. doi: 10.1016/j.bbalip.2016.01.015. PubMed DOI

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Adaptation of the late ISC pathway in the anaerobic mitochondrial organelles of Giardia intestinalis

. 2023 Oct ; 19 (10) : e1010773. [epub] 20231004

Structurally derived universal mechanism for the catalytic cycle of the tail-anchored targeting factor Get3

. 2022 Aug ; 29 (8) : 820-830. [epub] 20220718

Efficient CRISPR/Cas9-mediated gene disruption in the tetraploid protist Giardia intestinalis

. 2022 Apr ; 12 (4) : 210361. [epub] 20220427

Inheritance of the reduced mitochondria of Giardia intestinalis is coupled to the flagellar maturation cycle

. 2021 Sep 07 ; 19 (1) : 193. [epub] 20210907

The evolution of the Puf superfamily of proteins across the tree of eukaryotes

. 2020 Jun 30 ; 18 (1) : 77. [epub] 20200630

Mitochondrial dynamics in parasitic protists

. 2019 Nov ; 15 (11) : e1008008. [epub] 20191121

The Oxymonad Genome Displays Canonical Eukaryotic Complexity in the Absence of a Mitochondrion

. 2019 Oct 01 ; 36 (10) : 2292-2312.

A Single Tim Translocase in the Mitosomes of Giardia intestinalis Illustrates Convergence of Protein Import Machines in Anaerobic Eukaryotes

. 2018 Oct 01 ; 10 (10) : 2813-2822. [epub] 20181001

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...