Abstract
The concept of a phylogeny of parasites is inextricably linked to that of the phylogeny of eukaryotes. Though it can be useful to infer functional principles from similar morphologies and trophic strategies, the evolutionary histories of parasites are most accurately viewed as independent shifts to this lifestyle from a free-living state. This chapter will describe the phylogeny of eukaryotes, the evolutionary positions of various prominent parasites within this framework, and the ways in which genomics has facilitated understanding of the free-living to parasitic transition, both in terms of phylogeny and function. Two major cellular systems of parasitological relevance, mitochondrion-related organelles and endocytic systems, will be explored, highlighting where considering the genomics and molecular cell biology of parasites in the context of their emergence from free-living relatives have helped us to better understand organelle evolution.
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References
Abrahamsen MS, Templeton TJ, Enomoto S et al (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304:441–445. doi:10.1126/science.1094786
Ackers JP, Dhir V, Field MC (2005) A bioinformatic analysis of the RAB genes of Trypanosoma brucei. Mol Biochem Parasitol 141:89–97. doi:10.1016/j.molbiopara.2005.01.017
Adl SM, Simpson AG, Lane CE et al (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59:429–493. doi:10.1111/j.1550-7408.2012.00644.x
Adung’a VO, Gadelha C, Field MC (2013) Proteomic analysis of clathrin interactions in trypanosomes reveals dynamic evolution of endocytosis. Traffic 14:440–457. doi:10.1111/tra.12040
Agop-Nersesian C, Naissant B, Ben Rached F et al (2009) Rab11A-controlled assembly of the inner membrane complex is required for completion of apicomplexan cytokinesis. PLoS Pathog 5:e1000270. doi:10.1371/journal.ppat.1000270
Agop-Nersesian C, Egarter S, Langsley G et al (2010) Biogenesis of the inner membrane complex is dependent on vesicular transport by the alveolate specific GTPase Rab11B. PLoS Pathog 6:e1001029. doi:10.1371/journal.ppat.1001029
Ali M, Leung KF, Field MC (2014) The ancient small GTPase Rab21 functions in intermediate endocytic steps in trypanosomes. Eukaryot Cell 13:304–319. doi:10.1128/EC.00269-13
Allen JF (1993) Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J Theor Biol 165:609–631. doi:10.1006/jtbi.1993.1210
Allen CL, Goulding D, Field MC (2003) Clathrin-mediated endocytosis is essential in Trypanosoma brucei. EMBO J 22:4991–5002. doi:10.1093/emboj/cdg481
Allen CL, Liao D, Chung WL, Field MC (2007) Dileucine signal-dependent and AP-1-independent targeting of a lysosomal glycoprotein in Trypanosoma brucei. Mol Biochem Parasitol 156:175–190. doi:10.1016/j.molbiopara.2007.07.020
Angers CG, Merz AJ (2011) New links between vesicle coats and Rab-mediated vesicle targeting. Semin Cell Dev Biol 22:18–26. doi:10.1016/j.semcdb.2010.07.003
Bastida-Corcuera FD, Okumura CY, Colocoussi A, Johnson PJ (2005) Trichomonas vaginalis lipophosphoglycan mutants have reduced adherence and cytotoxicity to human ectocervical cells. Eukaryot Cell 4:1951–1958. doi:10.1128/EC.4.11.1951-1958.2005
Baum J, Gilberger TW, Frischknecht F, Meissner M (2008) Host-cell invasion by malaria parasites: insights from Plasmodium and Toxoplasma. Trends Parasitol 24:557–563. doi:10.1016/j.pt.2008.08.006
Björkholm P, Harish A, Hagström E et al (2015) Mitochondrial genomes are retained by selective constraints on protein targeting. Proc Natl Acad Sci 112:10154–10161. doi:10.1073/pnas.1421372112
Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166
Botero-Kleiven S, Fernández V, Lindh J et al (2001) Receptor-mediated endocytosis in an apicomplexan parasite (Toxoplasma gondii). Exp Parasitol 98:134–144. doi:10.1006/expr.2001.4624
Boxma B, de Graaf RM, van der Staay GW et al (2005) An anaerobic mitochondrion that produces hydrogen. Nature 434:74–79. doi:10.1038/nature03343
Boxma B, Ricard G, van Hoek AH et al (2007) The [FeFe] hydrogenase of Nyctotherus ovalis has a chimeric origin. BMC Evol Biol 7:230. doi:10.1186/1471-2148-7-230
Breinich MS, Ferguson DJ, Foth BJ et al (2009) A dynamin is required for the biogenesis of secretory organelles in Toxoplasma gondii. Curr Biol 19:277–286. doi:10.1016/j.cub.2009.01.039
Brighouse A, Dacks JB, Field MC (2010) Rab protein evolution and the history of the eukaryotic endomembrane system. Cell Mol Life Sci 67:3449–3465. doi:10.1007/s00018-010-0436-1
Briguglio JS, Kumar S, Turkewitz AP (2013) Lysosomal sorting receptors are essential for secretory granule biogenesis in Tetrahymena. J Cell Biol 203:537–550. doi:10.1083/jcb.201305086
Brown MW, Sharpe SC, Silberman JD et al (2013) Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. Proc R Soc 280:20131755. doi:10.1098/rspb.2013.1755
Brugerolle G, Bricheux G, Philippe H, Coffea G (2002) Collodictyon triciliatum and Diphylleia rotans (=Aulacomonas submarina) form a new family of flagellates (Collodictyonidae) with tubular mitochondrial cristae that is phylogenetically distant from other flagellate groups. Protist 153:59–70. doi:10.1078/1434-4610-00083
Burki F (2014) The eukaryotic tree of life from a global phylogenomic perspective. Cold Spring Harb Perspect Biol 6:a016147. doi:10.1101/cshperspect.a016147
Burki F, Corradi N, Sierra R et al (2013) Phylogenomics of the intracellular parasite Mikrocytos mackini reveals evidence for a mitosome in rhizaria. Curr Biol 23:1541–1547. doi:10.1016/j.cub.2013.06.033
Burri L, Williams BA, Bursac D et al (2006) Microsporidian mitosomes retain elements of the general mitochondrial targeting system. Proc Natl Acad Sci U S A 103:15916–15920. doi:10.1073/pnas.0604109103
Carlton JM, Hirt RP, Silva JC et al (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315:207–212. doi:10.1126/science.1132894
Cassera MB, Hazleton KZ, Riegelhaupt PM et al (2008) Erythrocytic adenosine monophosphate as an alternative purine source in Plasmodium falciparum. J Biol Chem 283:32889–32899. doi:10.1074/jbc.M804497200
Cavalier-Smith T (1987) Eukaryotes with no mitochondria. Nature 326:332–333. doi:10.1038/326332a0
Cavalier-Smith T (1989) Molecular phylogeny. Archaebacteria and Archezoa. Nature 339:l00–l01. doi:10.1038/339100a0
Cavalier-Smith T (2010) Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol Lett 6:342–345
Cavalier-Smith T, Chao EE (2004) Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.). Eur J Protistol 40:185–212. doi:10.1016/j.ejop.2004.01.002
Charneau S, Bastos IM, Mouray E et al (2007) Characterization of PfDYN2, a dynamin-like protein of Plasmodium falciparum expressed in schizonts. Microbes Infect 9:797–805. doi:10.1016/j.micinf.2007.02.020
Coppens I, Sinai AP, Joiner KA (2000) Toxoplasma gondii exploits host low-density lipoprotein receptor-mediated endocytosis for cholesterol acquisition. J Cell Biol 149:167–180. doi:10.1083/jcb.149.1.167
Cross GA (1975) Identification, purification and properties of clone-specific glycoprotein antigens constituting the surface coat of Trypanosoma brucei. Parasitology 71:393–417. doi:10.1017/S003118200004717X
Dell’Angelica EC (2009) AP-3-dependent trafficking and disease: the first decade. Curr Opin Cell Biol 21:552–559. doi:10.1016/j.ceb.2009.04.014
Delsuc F, Brinkmann H, Philippe H (2005) Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet 6:361–375. doi:10.1038/nrg1603
Denoeud F, Roussel M, Noel B et al (2011) Genome sequence of the stramenopile Blastocystis, a human anaerobic parasite. Genome Biol 12:R29. doi:10.1186/gb-2011-12-3-r29
Derelle R, Torruella G, Klimeš V et al (2015) Bacterial proteins pinpoint a single eukaryotic root. Proc Natl Acad Sci U S A 112:E693–E699. doi:10.1073/pnas.1420657112
Dou Z, McGovern OL, di Cristina M, Carruthers VB (2014) Toxoplasma gondii ingests and digests host cytosolic proteins. MBio 5:e01188–14. doi:10.1128/mBio.01188-14
Elde NC, Morgan G, Winey M et al (2005) Elucidation of clathrin-mediated endocytosis in tetrahymena reveals an evolutionarily convergent recruitment of dynamin. PLoS Genet 1:e52. doi:10.1371/journal.pgen.0010052
Elias M, Brighouse A, Gabernet-Castello C et al (2012) Sculpting the endomembrane system in deep time: high resolution phylogenetics of Rab GTPases. J Cell Sci 125:2500–2508. doi:10.1242/jcs.101378
Elliott DA, McIntosh MT, Hosgood HD et al (2008) Four distinct pathways of hemoglobin uptake in the malaria parasite Plasmodium falciparum. Proc Natl Acad Sci U S A 105:2463–2468. doi:10.1073/pnas.0711067105
Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440:623–630. doi:10.1038/nature04546
Eme L, Sharpe SC, Brown MW, Roger AJ (2014) On the age of eukaryotes: evaluating evidence from fossils and molecular clocks. Cold Spring Harb Perspect Biol 6:a016139. doi:10.1101/cshperspect.a016139
Faso C, Hehl AB (2011) Membrane trafficking and organelle biogenesis in Giardia lamblia: use it or lose it. Int J Parasitol 41:471–480. doi:10.1016/j.ijpara.2010.12.014
Field MC, Carrington M (2009) The trypanosome flagellar pocket. Nat Rev Microbiol 7:775–786. doi:10.1038/nrmicro2221
Field MC, Gabernet-Castello C, Dacks JB (2007) Reconstructing the evolution of the endocytic system: insights from genomics and molecular cell biology. Adv Exp Med Biol 607:84–96. doi:10.1007/978-0-387-74021-8_7
Field MC, Lumb JH, Adung’a VO et al (2009) Macromolecular trafficking and immune evasion in African trypanosomes. Int Rev Cell Mol Biol 278:1–67
Fomovska A, Huang Q, El Bissati K et al (2012) Novel N-benzoyl-2-hydroxybenzamide disrupts unique parasite secretory pathway. Antimicrob Agents Chemother 56:2666–2682. doi:10.1128/AAC.06450-11
Gabernet-Castello C, Dacks JB, Field MC (2009) The single ENTH-domain protein of trypanosomes; endocytic functions and evolutionary relationship with epsin. Traffic 10:894–911. doi:10.1111/j.1600-0854.2009.00910.x
García-Salcedo JA, Pérez-Morga D, Gijón P et al (2004) A differential role for actin during the life cycle of Trypanosoma brucei. EMBO J 23:780–789. doi:10.1038/sj.emboj.7600094
Gill EE, Diaz-Triviño S, Barberà MJ et al (2007) Novel mitochondrion-related organelles in the anaerobic amoeba Mastigamoeba balamuthi. Mol Microbiol 66:1306–1320. doi:10.1111/j.1365-2958.2007.05979.x
Gross U, Hambach C, Windeck T, Heesemann J (1993) Toxoplasma gondii: uptake of fetuin and identification of a 15-kDa fetuin-binding protein. Parasitol Res 79:191–194. doi:10.1007/BF00931891
Hackstein JHP (2005) Eukaryotic Fe-hydrogenases – old eukaryotic heritage or adaptive acquisitions? Biochem Soc Trans 33:47–50. doi:10.1042/BST0330047
Hackstein JHP, de Graaf RM, van Hellemond JJ, Tielens AGM (2008) Hydrogenosomes of Anaerobic Ciliates. In: Tachezy J (ed) Hydrog. Mitosomes Mitochondria Anaerob. Eukaryotes. Springer, Berlin/Heidelberg, pp 97–112
Hall B, Allen CL, Goulding D, Field MC (2004) Both of the Rab5 subfamily small GTPases of Trypanosoma brucei are essential and required for endocytosis. Mol Biochem Parasitol 138:67–77. doi:10.1016/j.molbiopara.2004.07.007
Hall BS, Pal A, Goulding D et al (2005) Trypanosoma brucei: TbRAB4 regulates membrane recycling and expression of surface proteins in procyclic forms. Exp Parasitol 111:160–171. doi:10.1016/j.exppara.2005.07.005
Hampl V, Silberman JD, Stechmann A et al (2008) Genetic evidence for a mitochondriate ancestry in the “amitochondriate” flagellate Trimastix pyriformis. PLoS One 3:e1383. doi:10.1371/journal.pone.0001383
Hampl V, Stairs CW, Roger AJ (2011) The tangled past of eukaryotic enzymes involved in anaerobic metabolism. Mob Genet Elements 1:71–74. doi:10.4161/mge.1.1.15588
He D, Fiz-Palacios O, Fu CJ et al (2014) An alternative root for the eukaryote tree of life. Curr Biol 24:465–470. doi:10.1016/j.cub.2014.01.036
Heiss AA, Walker G, Simpson AG (2013a) The flagellar apparatus of Breviata anathema, a eukaryote without a clear supergroup affinity. Eur J Protistol 49:354–372. doi:10.1016/j.ejop.2013.01.001
Heiss AA, Walker G, Simpson AG (2013b) The microtubular cytoskeleton of the apusomonad thecamonas, a sister lineage to the opisthokonts. Protist 164:598–621. doi:10.1016/j.protis.2013.05.005
Hirst J, Barlow LD, Francisco GC et al (2011) The fifth adaptor protein complex. PLoS Biol 9:e1001170. doi:10.1371/journal.pbio.1001170
Hirst J, Irving C, Borner GH (2013) Adaptor protein complexes AP-4 and AP-5: new players in endosomal trafficking and progressive spastic paraplegia. Traffic 14:153–164. doi:10.1111/tra.12028
Hirst J, Schlacht A, Norcott JP et al (2014) Characterization of TSET, an ancient and widespread membrane trafficking complex. Elife 3:e02866. doi:10.7554/eLife.02866
Honigberg BM, Mattern CF, Daniel WA (1971) Fine structure of the mastigont system in tritrichomonas foetus. J Protozool 18:183–198
Hrdy I, Hirt RP, Dolezal P et al (2004) Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432:618–622. doi:10.1038/nature03149
Hug LA, Stechmann A, Roger AJ (2010) Phylogenetic distributions and histories of proteins involved in anaerobic pyruvate metabolism in eukaryotes. Mol Biol Evol 27:311–324. doi:10.1093/molbev/msp237
Huotari J, Helenius A (2011) Endosome maturation. EMBO J 30:3481–3500. doi:10.1038/emboj.2011.286
Jackson AP, Otto TD, Aslett M et al (2016) Kinetoplastid phylogenomics reveals the evolutionary innovations associated with the origins of parasitism. Curr Biol 26:161–172. doi:10.1016/j.cub.2015.11.055
Jedelský PL, Doležal P, Rada P et al (2011) The minimal proteome in the reduced mitochondrion of the parasitic protist Giardia intestinalis. PLoS One 6:e17285. doi:10.1371/journal.pone.0017285
Jerlström-Hultqvist J, Einarsson E, Xu F et al (2013) Hydrogenosomes in the diplomonad Spironucleus salmonicida. Nat Commun 4:2493. doi:10.1038/ncomms3493
Juárez-Hernández LJ, García-Pérez RM, Salas-Casas A et al (2013) Entamoeba histolytica: the over expression of a mutated EhRabB protein produces a decrease of in vitro and in vivo virulence. Exp Parasitol 133:339–345. doi:10.1016/j.exppara.2012.12.008
Karnkowska A, Vacek V, Zubáčová Z et al (2016) Eukaryote without a Mitochondrial Organelle. Curr Biol 23;26(10):1274–84.
Katinka MD, Duprat S, Cornillot E et al (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450–453. doi:10.1038/35106579
Keithly J (2008) The mitochondrion-related organelle of cryptosporidium parvum. In: Tachezy J (ed) Hydrog. Mitosomes mitochondria anaerob. Eukaryotes. Springer, Berlin/Heidelberg, pp 231–253
Kibria KMK, Rawat K, Klinger CM et al (2015) A role for Adaptor Protein complex 1 in biogenesis and protein targeting to rhoptry organelles in Plasmodium falciparum. BBA Mol Cell Res 1853:699–710. doi:10.1016/j.bbamcr.2014.12.030
Klinger CM, Klute MJ, Dacks JB (2013a) Comparative genomic analysis of multi-subunit tethering complexes demonstrates an ancient pan-eukaryotic complement and sculpting in apicomplexa. PLoS One 8:e76278. doi:10.1371/journal.pone.0076278
Klinger CM, Nisbet RE, Ouologuem DT et al (2013b) Cryptic organelle homology in apicomplexan parasites: insights from evolutionary cell biology. Curr Opin Microbiol 16:424–431. doi:10.1016/j.mib.2013.07.015
Koumandou VL, Wickstead B, Ginger ML et al (2013) Molecular paleontology and complexity in the last eukaryotic common ancestor. Crit Rev Biochem Mol Biol 48:373–396. doi:10.3109/10409238.2013.821444
Krai P, Dalal S, Klemba M (2014) Evidence for a Golgi-to-endosome protein sorting pathway in Plasmodium falciparum. PLoS One 9:e89771. doi:10.1371/journal.pone.0089771
Kremer K, Kamin D, Rittweger E et al (2013) An overexpression screen of Toxoplasma gondii Rab-GTPases reveals distinct transport routes to the micronemes. PLoS Pathog 9:e1003213. doi:10.1371/journal.ppat.1003213
Langsley G, van Noort V, Carret C et al (2008) Comparative genomics of the Rab protein family in Apicomplexan parasites. Microbes Infect 10:462–470. doi:10.1016/j.micinf.2008.01.017
Lazarus MD, Schneider TG, Taraschi TF (2008) A new model for hemoglobin ingestion and transport by the human malaria parasite Plasmodium falciparum. J Cell Sci 121:1937–1949. doi:10.1242/jcs.023150
Li H, Han Z, Lu Y et al (2004) Isolation and functional characterization of a dynamin-like gene from Plasmodium falciparum. Biochem Biophys Res Commun 320:664–671. doi:10.1016/j.bbrc.2004.06.010
Lindmark DG, Müller M (1973) Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate tritrichomonas foetus, and its role in pyruvate metabolism. Biol Chem 248:7724–7728
Loftus B, Anderson I, Davies R et al (2005) The genome of the protist parasite Entamoeba histolytica. Nature 433:865–868. doi:10.1038/nature03291
Lukeš J, Flegontova O, Horák A (2015) Diplonemids. Curr Biol 25:R702–R704. doi:10.1016/j.cub.2015.04.052
Lumb JH, Leung KF, Dubois KN, Field MC (2011) Rab28 function in trypanosomes: interactions with retromer and ESCRT pathways. J Cell Sci 124:3771–3783. doi:10.1242/jcs.079178
Manna PT, Kelly S, Field MC (2013) Adaptin evolution in kinetoplastids and emergence of the variant surface glycoprotein coat in African trypanosomatids. Mol Phylogenet Evol 67:123–128. doi:10.1016/j.ympev.2013.01.002
Manna PT, Boehm C, Leung KF et al (2014) Life and times: synthesis, trafficking, and evolution of VSG. Trends Parasitol 30:251–258. doi:10.1016/j.pt.2014.03.004
Maralikova B, Ali V, Nakada-Tsukui K et al (2010) Bacterial-type oxygen detoxification and iron-sulfur cluster assembly in amoebal relict mitochondria. Cell Microbiol 12:331–342. doi:10.1111/j.1462-5822.2009.01397.x
Martincová E, Voleman L, Pyrih J et al (2015) Probing the biology of Giardia intestinalis mitosomes using in vivo enzymatic tagging. Mol Cell Biol 35:2864–2874. doi:10.1128/MCB.00448-15
Meyer J (2007) [FeFe] hydrogenases and their evolution: a genomic perspective. Cell Mol Life Sci 64:1063–1084. doi:10.1007/s00018-007-6477-4
Mi-ichi F, Abu Yousuf M, Nakada-Tsukui K, Nozaki T (2009) Mitosomes in Entamoeba histolytica contain a sulfate activation pathway. Proc Natl Acad Sci U S A 106:21731–21736. doi:10.1073/pnas.0907106106
Miranda K, Pace DA, Cintron R et al (2010) Characterization of a novel organelle in Toxoplasma gondii with similar composition and function to the plant vacuole. Mol Microbiol 76:1358–1375. doi:10.1111/j.1365-2958.2010.07165.x
Mogi T, Kita K (2010) Diversity in mitochondrial metabolic pathways in parasitic protists Plasmodium and Cryptosporidium. Parasitol Int 59:305–312. doi:10.1016/j.parint.2010.04.005
Morgan GW, Goulding D, Field MC (2004) The single dynamin-like protein of Trypanosoma brucei regulates mitochondrial division and is not required for endocytosis. J Biol Chem 279:10692–10701. doi:10.1074/jbc.M312178200
Morrison HG, McArthur AG, Gillin FD et al (2007) Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317:1921–1926
Müller M, Mentel M, van Hellemond JJ et al (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76:444–495. doi:10.1128/MMBR.05024-11
Nevin WD, Dacks JB (2009) Repeated secondary loss of adaptin complex genes in the Apicomplexa. Parasitol Int 58:86–94. doi:10.1016/j.parint.2008.12.002
Ngô HM, Yang M, Paprotka K et al (2003) AP-1 in Toxoplasma gondii mediates biogenesis of the rhoptry secretory organelle from a post-Golgi compartment. J Biol Chem 278:5343–5352. doi:10.1074/jbc.M208291200
Ngô HM, Yang M, Joiner KA (2004) Are rhoptries in Apicomplexan parasites secretory granules or secretory lysosomal granules? Mol Microbiol 52:1531–1541. doi:10.1111/j.1365-2958.2004.04056.x
Nichols BA, Chiappino ML, Pavesio CE (1994) Endocytosis at the micropore of Toxoplasma gondii. Parasitol Res 80:91–98
Nývltová E, Šuták R, Harant K et al (2013) NIF-type iron-sulfur cluster assembly system is duplicated and distributed in the mitochondria and cytosol of Mastigamoeba balamuthi. Proc Natl Acad Sci U S A 110:7371–7376. doi:10.1073/pnas.1219590110
Nývltová E, Stairs CW, Hrdý I et al (2015) Lateral gene transfer and gene duplication played a key role in the evolution of Mastigamoeba balamuthi hydrogenosomes. Mol Biol Evol 32:1039–1055. doi:10.1093/molbev/msu408
Okamoto N, Keeling PJ (2014) The 3D structure of the apical complex and association with the flagellar apparatus revealed by serial TEM tomography in Psammosa pacifica, a distant relative of the Apicomplexa. PLoS One 9:e84653. doi:10.1371/journal.pone.0084653
Okumura CY, Baum LG, Johnson PJ (2008) Galectin-1 on cervical epithelial cells is a receptor for the sexually transmitted human parasite Trichomonas vaginalis. Cell Microbiol 10:2078–2090. doi:10.1111/j.1462-5822.2008.01190.x
Pal A, Hall BS, Jeffries TR, Field MC (2003) Rab5 and Rab11 mediate transferrin and anti-variant surface glycoprotein antibody recycling in Trypanosoma brucei. Biochem J 374:443–451. doi:10.1042/BJ20030469
Parussini F, Coppens I, Shah PP et al (2010) Cathepsin L occupies a vacuolar compartment and is a protein maturase within the endo/exocytic system of Toxoplasma gondii. Mol Microbiol 76:1340–1357. doi:10.1111/j.1365-2958.2010.07181.x
Perdomo D, Aït-Ammar N, Syan S et al (2015) Cellular and proteomics analysis of the endomembrane system from the unicellular Entamoeba histolytica. J Proteomics 112C:125–140. doi:10.1016/j.jprot.2014.07.034
Philippe H (2000) Opinion: long branch attraction and protist phylogeny. Protist 151:307–316. doi:10.1078/S1434-4610(04)70029-2
Philippe H, Brinkmann H, Lavrov DV et al (2011) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 9:e1000602. doi:10.1371/journal.pbio.1000602
Pieperhoff MS, Schmitt M, Ferguson DJ, Meissner M (2013) The role of clathrin in post-golgi trafficking in Toxoplasma gondii. PLoS One 8:e77620. doi:10.1371/journal.pone.0077620
Plattner F, Soldati-Favre D (2008) Hijacking of host cellular functions by the Apicomplexa. Annu Rev Microbiol 62:471–487. doi:10.1146/annurev.micro.62.081307.162802
Popot JL, de Vitry C (1999) On the microassembly of integral membrane proteins. Annu Rev Biophys Biophys Chem 19:369–403
Putignani L, Tait A, Smith HV et al (2004) Characterization of a mitochondrion-like organelle in Cryptosporidium parvum. Parasitology 129:1–18. doi:10.1017/S003118200400527X
Rao Y, Rückert C, Saenger W, Haucke V (2012) The early steps of endocytosis: from cargo selection to membrane deformation. Eur J Cell Biol 91:226–233. doi:10.1016/j.ejcb.2011.02.004
Reider A, Wendland B (2011) Endocytic adaptors – social networking at the plasma membrane. J Cell Sci 124:1613–1622. doi:10.1242/jcs.073395
Robinson MS (2004) Adaptable adaptors for coated vesicles. Trends Cell Biol 14:167–174. doi:10.1016/j.tcb.2004.02.002
Rodríguez-Ezpeleta N, Brinkmann H, Roure B et al (2007) Detecting and overcoming systematic errors in genome-scale phylogenies. Syst Biol 56:389–399. doi:10.1080/10635150701397643
Rosati G, Modeo L (2003) Extrusomes in ciliates: diversification, distribution, and phylogenetic implications. J Eukaryot Microbiol 50:383–402
Schlacht A, Mowbrey K, Elias M et al (2013) Ancient complexity, opisthokont plasticity, and discovery of the 11th subfamily of Arf GAP proteins. Traffic 14:636–649. doi:10.1111/tra.12063
Scott CC, Vacca F, Gruenberg J (2014) Endosome maturation, transport and functions. Semin Cell Dev Biol 31:2–10. doi:10.1016/j.semcdb.2014.03.034
Sigala PA, Goldberg DE (2014) The peculiarities and paradoxes of plasmodium heme metabolism. Annu Rev Microbiol 68:259–278. doi:10.1146/annurev-micro-091313-103537
Silverman JS, Schwartz KJ, Hajduk SL, Bangs JD (2011) Late endosomal Rab7 regulates lysosomal trafficking of endocytic but not biosynthetic cargo in Trypanosoma brucei. Mol Microbiol 82:664–678. doi:10.1111/j.1365-2958.2011.07842.x
Simpson AG (2003) Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). Int J Syst Evol Microbiol 53:1759–1777. doi:10.1099/ijs.0.02578-0
Sloves PJ, Delhaye S, Mouveaux T et al (2012) Toxoplasma sortilin-like receptor regulates protein transport and is essential for apical secretory organelle biogenesis and host infection. Cell Host Microbe 11:515–527. doi:10.1016/j.chom.2012.03.006
Sogin ML (1991) Early evolution and the origin of eukaryotes. Curr Opin Genet Dev 1:457–463. doi:10.1016/S0959-437X(05)80192-3
Stairs CW, Roger AJ, Hampl V (2011) Eukaryotic pyruvate formate lyase and its activating enzyme were acquired laterally from a firmicute. Mol Biol Evol 28:2087–2099. doi:10.1093/molbev/msr032
Stairs CW, Eme L, Brown MW et al (2014) A SUF Fe-S cluster biogenesis system in the mitochondrion-related organelles of the anaerobic protist Pygsuia. Curr Biol 24:1176–1186. doi:10.1016/j.cub.2014.04.033
Stechmann A, Hamblin K, Pérez-Brocal V et al (2008) Organelles in blastocystis that blur the distinction between mitochondria and hydrogenosomes. Curr Biol 18:580–585. doi:10.1016/j.cub.2008.03.037
Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513–525. doi:10.1038/nrm2728
Stiller JW, Hall BD (1999) Long-branch attraction and the rDNA model of early eukaryotic evolution. Mol Biol Evol 16:1270–1279. doi:10.1093/oxfordjournals.molbev.a026217
Tomavo S (2014) Evolutionary repurposing of endosomal systems for apical organelle biogenesis in Toxoplasma gondii. Int J Parasitol 44:133–138. doi:10.1016/j.ijpara.2013.10.003
Tomavo S, Slomianny C, Meissner M, Carruthers VB (2013) Protein trafficking through the endosomal system prepares intracellular parasites for a home invasion. PLoS Pathog 9:e1003629. doi:10.1371/journal.ppat.1003629
Tovar J, León-Avila G, Sánchez LB et al (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426:172–176. doi:10.1038/nature01945
Traub LM, Bonifacino JS (2013) Cargo recognition in clathrin-mediated endocytosis. Cold Spring Harb Perspect Biol 5:a016790. doi:10.1101/cshperspect.a016790
Twu O, de Miguel N, Lustig G et al (2013) Trichomonas vaginalis exosomes deliver cargo to host cells and mediate host: parasite interactions. PLoS Pathog 9, e1003482. doi:10.1371/journal.ppat.1003482
Upcroft P, Upcroft JA (2001) Drug targets and mechanisms of resistance in the anaerobic protozoa. Clin Microbiol Rev 14:150–164. doi:10.1128/CMR.14.1.150-164.2001
van Dooren GG, Reiff SB, Tomova C et al (2009) A novel dynamin-related protein has been recruited for apicoplast fission in Toxoplasma gondii. Curr Biol 19:267–276. doi:10.1016/j.cub.2008.12.048
Vanderheyden N, Wong J, Docampo R (2000) A pyruvate-proton symport and an H + −ATPase regulate the intracellular pH of Trypanosoma brucei at different stages of its life cycle. Biochem J 346(Pt 1):53–62. doi:10.1042/0264-6021:3470887
Vickerman K (1969) On the surface coat and flagellar adhesion in trypanosomes. J Cell Sci 5:163–193
Woo YH, Ansari H, Otto TD et al (2015) Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites. Elife 4:e06974. doi:10.7554/eLife.06974
Woodrow CJ, Burchmore RJ, Krishna S (2000) Hexose permeation pathways in Plasmodium falciparum-infected erythrocytes. Proc Natl Acad Sci U S A 97:9931–9936. doi:10.1073/pnas.170153097
Yubuki N, Leander BS (2013) Evolution of microtubule organizing centers across the tree of eukaryotes. Plant J 75:230–244. doi:10.1111/tpj.12145
Zhao S, Burki F, Bråte J et al (2012) Collodictyon – an ancient lineage in the tree of eukaryotes. Mol Biol Evol 29:1557–1568. doi:10.1093/molbev/mss001
Zubáčová Z, Novák L, Bublíková J et al (2013) The mitochondrion-like organelle of trimastix pyriformis contains the complete glycine cleavage system. PLoS One 8, e55417. doi:10.1371/journal.pone.0055417
Funding
AK was supported by the European Social Fund and the state budget of the Czech Republic, project no. CZ.1.07/2.3.00/30.0061. VH was supported by Czech Science foundation projects P506-12-1010 and GAP506/11/1317 and by the Ministry of Education, Youth and Sports of CR within the National Sustainability Program II (Project BIOCEV-FAR ) LQ1604 and by the project ‘‘BIOCEV’’ (CZ.1.05/1.1.00/02.0109), from the European Regional Development Fund. CMK is funded by graduate studentships from the Women and Children’s Health Research Institute, Alberta Innovates Health Solutions, and the Canadian Institutes of Health Research. EKH is funded by a Vanier Canada Graduate Scholarship and an Alberta Innovates – Health Solutions Graduate Studentship. Work from the Dacks laboratory is supported by an Alberta Innovates Technology Futures New Faculty Award and by Natural Science and Engineering Research Council of Canada (NSERC) Discovery Grants RES0021028. JBD is the Canada Research Chair (Tier II) in Evolutionary Cell Biology.
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Klinger, C.M., Karnkowska, A., Herman, E.K., Hampl, V., Dacks, J.B. (2016). Phylogeny and Evolution. In: Walochnik, J., Duchêne, M. (eds) Molecular Parasitology. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1416-2_12
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