Abstract
Among all apicomplexans, the mitochondrion-related organelle of Cryptosporidium species is the least studied. To date, most of our knowledge on this tiny organelle stems from observations on the remnant mitochondrion, mitosome, of Cryptosporidium parvum. In C. parvum the mitosome is structurally distinguished from the hydrogenosomes and mitosomes of other anaerobic protists by its (1) close association with the crystalloid body, an organelle unique to this apicomplexan and the function of which is currently unknown; (2) close association with the outer nuclear membrane and possibly nuclear pores; (3) envelopment by rough endoplasmic reticulum and in some cases an apparent direct tethering to ribosomes; and (4) atypical internal membranous compartments that lack well-defined crista junctions with the mitochondrial inner membrane, a characteristic that defines most aerobic mitochondria. Like most hydrogenosome- and other mitosome-bearing anaerobic protists, however, C. parvum lacks a mitochondrial genome, i.e. proteins are encoded by the nucleus and targeted back to the mitosome. As a consequence of this reductive evolution, there are no genes for electron transport or oxidative phosphorylation, and the only function so far ascribed to this tiny organelle is one common to all eukaryotic mitochondria, the assembly and maturation of iron-sulphur clusters. The ultrastructure and tomography of the C. parvum mitosome and crystalloid body, as well as the probable functions of these organelles, are the primary topics herein. An overview of iron-sulphur cluster biosynthesis, likely mechanisms for import into and export from the mitosome, as well as core carbohydrate and energy metabolism is also discussed. Similarities and differences in the structure and function of both organelles in the genus Cryptosporidium, with anaerobic protists in general, and with other apicomplexans specifically, are described.
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References
Abrahamsen MS (2001) Cryptosporidium parvum genome project. Comp Funct Genomics 2(1):19–21. https://doi.org/10.1002/cfg.67
Abrahamsen MS, Templeton TJ, Enomoto S et al (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304(5669):441–445. https://doi.org/10.1126/science.1094786
Aji T, Flanigan T, Marshall R et al (1991) Ultrastructural study of asexual development of Cryptosporidium parvum in a human intestinal cell line. J Protozool 38(6):82S–84S
Alcock F, Webb CT, Dolezal P et al (2012) A small Tim homohexamer in the relict mitochondrion of cryptosporidium. Mol Biol Evol 29(1):113–122. https://doi.org/10.1093/molbev/msr165
Alvarez-Pellitero P, Quiroga MI, Sitja-Bobadilla A et al (2004) Cryptosporidium scophthalmi n. Sp. (Apicomplexa: Cryptosporidiidae) from cultured turbot Scophthalmus maximus. Light and electron microscope description and histopathological study. Dis Aquat Org 62(1–2):133–145. https://doi.org/10.3354/dao062133
Beyer TV, Svezhova NV, Sidorenko NV et al (2000) Cryptosporidium parvum (Coccidia, apicomplexa): some new ultrastructural observations on its endogenous development. Eur J Protistol 36(2):151–159. https://doi.org/10.1016/S0932-4739(00)80034-6
Boxma B, de Graaf RM, van der Staay GW et al (2005) An anaerobic mitochondrion that produces hydrogen. Nature 434(7029):74–79
Braymer JJ, Lill R (2017) Iron-sulfur cluster biogenesis and trafficking in mitochondria. J Biol Chem 292(31):12754–12763. https://doi.org/10.1074/jbc.R117.787101
Brown JR, Doolittle WF (1997) Archaea and the prokaryote-to-eukaryote transition. Microbiol Mol Biol Rev 61(4):456–502
Cai X, Fuller AL, McDougald LR et al (2003) Apicoplast genome of the coccidian Eimeria tenella. Gene 321:39–46. https://doi.org/10.1016/j.gene.2003.08.008
Cai X, Herschap D, Zhu G (2005) Functional characterization of an evolutionarily distinct phosphopantetheinyl transferase in the apicomplexan Cryptosporidium parvum. Eukaryot Cell 4(7):1211–1220. https://doi.org/10.1128/EC.4.7.1211-1220.2005
Cavalier-Smith T (2014) Gregarine site-heterogeneous 18S rDNA trees, revision of gregarine higher classification, and the evolutionary diversification of Sporozoa. Eur J Protistol 50(5):472–495. https://doi.org/10.1016/j.ejop.2014.07.002
Chan KW, Slotboom DJ, Cox S et al (2005) A novel ADP/ATP transporter in the Mitosome of the Microaerophilic human parasite Entamoeba histolytica. Curr Biol 15(8):737–742
Clark CG, Roger AJ (1995) Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc Natl Acad Sci U S A 92(14):6518–6521
Crawford MJ, Fraunholz MJ, Roos D (2003) Energy Metabolism in the Apicomplexa. In: Marr JJ, Nielsen TW, Kouiecki RW (eds) Molecular Medical parasitology, vol 7. Academic, New York, pp 154–169
Csordas G, Renken C, Varnai P et al (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174(7):915–921. https://doi.org/10.1083/jcb.200604016
Ctrnacta V, Ault JG, Stejskal F et al (2006) Localization of pyruvate:NADP+ oxidoreductase in sporozoites of Cryptosporidium parvum. J Eukaryot Microbiol 53(4):225–231. https://doi.org/10.1111/j.1550-7408.2006.00099.x
Dean P, Sendra KM, Williams TA et al (2018) Transporter gene acquisition and innovation in the evolution of Microsporidia intracellular parasites. Nat Commun 9(1):1709. https://doi.org/10.1038/s41467-018-03923-4
Deng Y, Marko M, Buttle KF et al (1999) Cubic membrane structure in amoeba (Chaos carolinensis) mitochondria determined by electron microscopic tomography. J Struct Biol 127(3):231–239. https://doi.org/10.1006/jsbi.1999.4147
Desportes I, Schrével J (2013) Treatise on zoology - anatomy, taxonomy, biology. The gregarines. The early branching Apicomplexa. BRILL, Leiden
Dolezal P, Smid O, Rada P et al (2005) Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc Natl Acad Sci U S A 102(31):10924–10929
Dolezal P, Likic V, Tachezy J et al (2006) Evolution of the molecular machines for protein import into mitochondria. Science 313(5785):314–318
Dolezal P, Dagley MJ, Kono M et al (2010) The essentials of protein import in the degenerate mitochondrion of Entamoeba histolytica. PLoS Pathog 6(3):e1000812. https://doi.org/10.1371/journal.ppat.1000812
Ellis JE, Setchell KD, Kaneshiro ES (1994) Detection of ubiquinone in parasitic and free-living protozoa, including species devoid of mitochondria. Mol Biochem Parasitol 65(2):213–224. https://doi.org/10.1016/0166-6851(94)90073-6
Embley TM, van der Giezen M, Horner DS et al (2003) Mitochondria and hydrogenosomes are two forms of the same fundamental organelle. Philos Trans R Soc Lond Ser B Biol Sci 358(1429):191–201; discussion 201–202. https://doi.org/10.1098/rstb.2002.1190
Entrala E, Mascaro C (1997) Glycolytic enzyme activities in Cryptosporidium parvum oocysts. FEMS Microbiol Lett 151(1):51–57. https://doi.org/10.1111/j.1574-6968.1997.tb10393.x
Fayer R, Xiao L (2007) Cryptosporidium and cryptosporidiosis. CRC Press
Fenchel T, Perry T, Thane A (1977) Anaerobiosis and symbiosis with bacteria in free-living ciliates. J Protozool 24(1):154–163
Freibert SA, Goldberg AV, Hacker C et al (2017) Evolutionary conservation and in vitro reconstitution of microsporidian iron-sulfur cluster biosynthesis. Nat Commun 8:13932. https://doi.org/10.1038/ncomms13932
Frey TG, Perkins GA, Ellisman MH (2006) Electron tomography of membrane-bound cellular organelles. Annu Rev Biophys Biomol Struct 35:199–224. https://doi.org/10.1146/annurev.biophys.35.040405.102039
Fry M, Beesley JE (1991) Mitochondria of mammalian Plasmodium spp. Parasitology 102(Pt 1):17–26
Gentle IE, Perry AJ, Alcock FH, Likić VA, Dolezal P, Ng ET, Purcell AW, McConnville M, Naderer T, Chanez AL, Charrière F, Aschinger C, Schneider A, Tokatlidis K, Lithgow T (2007) Conserved motifs reveal details of ancestry and structure in the small TIM chaperones of the mitochondrial intermembrane space. Mol Biol Evol 24(5):1149–1160
Goldberg AV, Molik S, Tsaousis AD et al (2008) Localization and functionality of microsporidian iron-Sulphur cluster assembly proteins. Nature 452(7187):624–628. https://doi.org/10.1038/nature06606
Harris JR, Scheffler D (2002) Routine preparation of air-dried negatively stained and unstained specimens on holey carbon support films: a review of applications. Micron 33(5):461–480. https://doi.org/10.1016/S0968-4328(01)00039-7
Henriquez FL, Richards TA, Roberts F et al (2005) The unusual mitochondrial compartment of Cryptosporidium parvum. Trends Parasitol 21(2):68–74. https://doi.org/10.1016/j.pt.2004.11.010
Horner DS, Foster PG, Embley TM (2000) Iron hydrogenases and the evolution of anaerobic eukaryotes. Mol Biol Evol 17(11):1695–1709
Inui H, Ono K, Miyatake K et al (1987) Purification and characterization of pyruvate:NADP+ oxidoreductase in Euglena gracilis. J Biol Chem 262(19):9130–9135
Jerlstrom-Hultqvist J, Einarsson E, Xu F et al (2013) Hydrogenosomes in the diplomonad Spironucleus salmonicida. Nat Commun 4:2493. https://doi.org/10.1038/ncomms3493
Johnson E, Cascio D, Sawaya MR et al (2005) Crystal structures of a tetrahedral open pore ferritin from the hyperthermophilic archaeon Archaeoglobus fulgidus. Structure 13(4):637–648. https://doi.org/10.1016/j.str.2005.01.019
Katinka MD, Duprat S, Cornillot E et al (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414(6862):450–453
Kayser O, Waters WR, Woods KM et al (2002) Evaluation of in vitro and in vivo activity of benzindazole-4,9-quinones against Cryptosporidium parvum. J Antimicrob Chemother 50(6):975–980
Keeling PJ (2004) Reduction and compaction in the genome of the apicomplexan parasite Cryptosporidium parvum. Dev Cell 6(5):614–616. https://doi.org/10.1016/S1534-5807(04)00135-2
Keeling PJ, Fast NM (2002) Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu Rev Microbiol 56:93–116
Keithly JS, Langreth SG, Buttle KF et al (2005) Electron tomographic and ultrastructural analysis of the Cryptosporidium parvum relict mitochondrion, its associated membranes, and organelles. J Eukaryot Microbiol 52(2):132–140. https://doi.org/10.1111/j.1550-7408.2005.04-3317.x
Kita K, Hirawake H, Miyadera H et al (2002) Role of complex II in anaerobic respiration of the parasite mitochondria from Ascaris suum and Plasmodium falciparum. Biochim Biophys Acta 1553(1–2):123–139. https://doi.org/10.1016/S0005-2728(01)00237-7
Krungkrai J, Burat D, Kudan S et al (1999) Mitochondrial oxygen consumption in asexual and sexual blood stages of the human malarial parasite, Plasmodium falciparum. Southeast Asian J Trop Med Public Health 30(4):636–642
Krungkrai J, Prapunwattana P, Krungkrai SR (2000) Ultrastructure and function of mitochondria in gametocytic stage of Plasmodium falciparum. Parasite 7(1):19–26. https://doi.org/10.1051/parasite/2000071019
LaGier MJ, Tachezy J, Stejskal F et al (2003) Mitochondrial-type iron-sulfur cluster biosynthesis genes (IscS and IscU) in the apicomplexan Cryptosporidium parvum. Microbiology 149(Pt 12):3519–3530. https://doi.org/10.1099/mic.0.26365-0
Lantsman Y, Tan KS, Morada M et al (2008) Biochemical characterization of a mitochondrial-like organelle from Blastocystis sp. subtype 7. Microbiology 154.(Pt 9:2757–2766. https://doi.org/10.1099/mic.0.2008/017897-0
Leon-Avila G, Tovar J (2004) Mitosomes of Entamoeba histolytica are abundant mitochondrion-related remnant organelles that lack a detectable organellar genome. Microbiology 150(Pt 5):1245–1250
Lill R, Dutkiewicz R, Freibert SA et al (2015) The role of mitochondria and the CIA machinery in the maturation of cytosolic and nuclear iron-sulfur proteins. Eur J Cell Biol 94(7–9):280–291. https://doi.org/10.1016/j.ejcb.2015.05.002
Lithgow T, Schneider A (2010) Evolution of macromolecular import pathways in mitochondria, hydrogenosomes and mitosomes. Philos Trans R Soc Lond Ser B Biol Sci 365(1541):799–817. https://doi.org/10.1098/rstb.2009.0167
Liu S, Roellig DM, Guo Y et al (2016) Evolution of mitosome metabolism and invasion-related proteins in Cryptosporidium. BMC Genomics 17(1):1006–016-3343-5. https://doi.org/10.1186/s12864-016-3343-5
Lucic V, Forster F, Baumeister W (2005) Structural studies by electron tomography: from cells to molecules. Annu Rev Biochem 74:833–865. https://doi.org/10.1146/annurev.biochem.73.011303.074112
Lucic V, Rigort A, Baumeister W (2013) Cryo-electron tomography: the challenge of doing structural biology in situ. J Cell Biol 202(3):407–419. https://doi.org/10.1083/jcb.201304193
Lukes J (1992) Life cycle of Goussia pannonica (Molnar, 1989) (Apicomplexa, Eimeriorina), an Extracytoplasmic Coccidium from the white bream Blicca bjoerkna. J Protozool 39(4):484–494. https://doi.org/10.1111/j.1550-7408.1992.tb04836.x
Madern D, Cai X, Abrahamsen MS et al (2004) Evolution of Cryptosporidium parvum lactate dehydrogenase from malate dehydrogenase by a very recent event of gene duplication. Mol Biol Evol 21(3):489–497. https://doi.org/10.1093/molbev/msh042
Mannella CA (2006) The relevance of mitochondrial membrane topology to mitochondrial function. Biochim Biophys Acta 1762(2):140–147. https://doi.org/10.1016/j.bbadis.2005.07.001
Mannella CA, Pfeiffer DR, Bradshaw PC et al (2001) Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications. IUBMB Life 52(3–5):93–100. https://doi.org/10.1080/15216540152845885
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(3):331–342. https://doi.org/10.1111/j.1462-5822.2009.01397.x
Mauzy MJ, Enomoto S, Lancto CA et al (2012) The Cryptosporidium parvum transcriptome during in vitro development. PLoS One 7(3):e31715. https://doi.org/10.1371/journal.pone.0031715
Melo EJ, Attias M, De Souza W (2000) The single mitochondrion of tachyzoites of Toxoplasma gondii. J Struct Biol 130(1):27–33. https://doi.org/10.1006/jsbi.2000.4228
Mi-Ichi F, Takeo S, Takashima E et al (2003) Unique properties of respiratory chain in Plasmodium falciparum mitochondria. Adv Exp Med Biol 531:117–133
Miller CN, Josse L, Brown I et al (2018a) A cell culture platform for Cryptosporidium that enables long-term cultivation and new tools for the systematic investigation of its biology. Int J Parasitol 48(3–4):197–201. https://doi.org/10.1016/j.ijpara.2017.10.001
Miller CN, Josse L, Tsaousis AD (2018b) Localization of Fe-S biosynthesis machinery in Cryptosporidium parvum Mitosome. J Eukaryot Microbiol 65:913. https://doi.org/10.1111/jeu.12663
Mogi T, Kita K (2010) Diversity in mitochondrial metabolic pathways in parasitic protists Plasmodium and Cryptosporidium. Parasitol Int 59(3):305–312. https://doi.org/10.1016/j.parint.2010.04.005
Muller M, Mentel M, van Hellemond JJ et al (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76(2):444–495. https://doi.org/10.1128/MMBR.05024-11
Nakazawa M, Inui H, Yamaji R et al (2000) The origin of pyruvate: NADP+ oxidoreductase in mitochondria of Euglena gracilis. FEBS Lett 479(3):155–156
Nasirudeen AM, Tan KS (2004) Isolation and characterization of the mitochondrion-like organelle from Blastocystis hominis. J Microbiol Methods 58(1):101–109
Ovciarikova J, Lemgruber L, Stilger KL et al (2017) Mitochondrial behaviour throughout the lytic cycle of Toxoplasma gondii. Sci Rep 7:42746. https://doi.org/10.1038/srep42746
Painter HJ, Morrisey JM, Mather MW et al (2007) Specific role of mitochondrial electron transport in blood-stage Plasmodium falciparum. Nature 446(7131):88–91. https://doi.org/10.1038/nature05572
Petry F, Harris JR (1999) Ultrastructure, fractionation and biochemical analysis of Cryptosporidium parvum sporozoites. Int J Parasitol 29(8):1249–1260. https://doi.org/10.1016/S0020-7519(99)00080-6
Putignani L, Tait A, Smith HV et al (2004) Characterization of a mitochondrion-like organelle in Cryptosporidium parvum. Parasitology 129(Pt 1):1–18
Richardson E, Zerr K, Tsaousis A et al (2015) Evolutionary cell biology: functional insight from “endless forms most beautiful”. Mol Biol Cell 26(25):4532–4538. https://doi.org/10.1091/mbc.E14-10-1433
Riordan CE, Langreth SG, Sanchez LB et al (1999) Preliminary evidence for a mitochondrion in Cryptosporidium parvum: phylogenetic and therapeutic implications. J Eukaryot Microbiol 46(5):52S–55S
Riordan CE, Ault JG, Langreth SG et al (2003) Cryptosporidium parvum Cpn60 targets a relict organelle. Curr Genet 44(3):138–147. https://doi.org/10.1007/s00294-003-0432-1
Roberts CW, Roberts F, Henriquez FL et al (2004) Evidence for mitochondrial-derived alternative oxidase in the apicomplexan parasite Cryptosporidium parvum: a potential anti-microbial agent target. Int J Parasitol 34(3):297–308. https://doi.org/10.1016/j.ijpara.2003.11.002
Rotte C, Stejskal F, Zhu G et al (2001) Pyruvate: NADP+ oxidoreductase from the mitochondrion of Euglena gracilis and from the apicomplexan Cryptosporidium parvum: a biochemical relic linking pyruvate metabolism in mitochondriate and amitochondriate protists. Mol Biol Evol 18(5):710–720. https://doi.org/10.1093/oxfordjournals.molbev.a003853
Ryan U, Paparini A, Monis P et al (2016) It's official – Cryptosporidium is a gregarine: what are the implications for the water industry? Water Res 105:305–313. https://doi.org/10.1016/j.watres.2016.09.013
Schneider A, Bursac D, Lithgow T (2008) The direct route: a simplified pathway for protein import into the mitochondrion of trypanosomes. Trends Cell Biol 18(1):12–18. https://doi.org/10.1016/j.tcb.2007.09.009
Senkovich O, Speed H, Grigorian A et al (2005) Crystallization of three key glycolytic enzymes of the opportunistic pathogen Cryptosporidium parvum. Biochim Biophys Acta 1750(2):166–172. https://doi.org/10.1016/j.bbapap.2005.04.009
Siddall ME, Desser SS (1992) Ultrastructure of gametogenesis and Sporogony of Haemogregarina (sensu lato) myoxocephali (Apicomplexa: Adeleina) in the marine leech Malmiana scorpii. J Protozool 39(5):545–554. https://doi.org/10.1111/j.1550-7408.1992.tb04849.x
Slapeta J, Keithly JS (2004) Cryptosporidium parvum mitochondrial-type HSP70 targets homologous and heterologous mitochondria. Eukaryot Cell 3(2):483–494
Stejskal F, Slapeta J, Ctrnacta V et al (2003) A Narf-like gene from Cryptosporidium parvum resembles homologues observed in aerobic protists and higher eukaryotes. FEMS Microbiol Lett 229(1):91–96. https://doi.org/10.1016/S0378-1097(03)00794-8
Suzuki T, Hashimoto T, Yabu Y et al (2004) Direct evidence for cyanide-insensitive quinol oxidase (alternative oxidase) in apicomplexan parasite Cryptosporidium parvum: phylogenetic and therapeutic implications. Biochem Biophys Res Commun 313(4):1044–1052. https://doi.org/10.1016/j.bbrc.2003.12.038
Tan KS (2008) New insights on classification, identification, and clinical relevance of Blastocystis spp. Clin Microbiol Rev 21(4):639–665. https://doi.org/10.1128/CMR.00022-08
Templeton TJ, Iyer LM, Anantharaman V et al (2004) Comparative analysis of apicomplexa and genomic diversity in eukaryotes. Genome Res 14(9):1686–1695. https://doi.org/10.1101/gr.2615304
Templeton TJ, Enomoto S, Chen WJ et al (2010) A genome-sequence survey for Ascogregarina taiwanensis supports evolutionary affiliation but metabolic diversity between a gregarine and Cryptosporidium. Mol Biol Evol 27(2):235–248. https://doi.org/10.1093/molbev/msp226
Tetley L, Brown SM, McDonald V et al (1998) Ultrastructural analysis of the sporozoite of Cryptosporidium parvum. Microbiology 144. ( Pt 12)(Pt 12:3249–3255. https://doi.org/10.1099/00221287-144-12-3249
Thompson RC, Olson ME, Zhu G et al (2005) Cryptosporidium and cryptosporidiosis. Adv Parasitol 59:77–158
Tovar J, Fischer A, Clark CG (1999) The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol Microbiol 32(5):1013–1021
Tovar J, Leon-Avila G, Sanchez LB et al (2003) Mitochondrial remnant organelles of Giardia function in iron-Sulphur protein maturation. Nature 426(6963):172–176
Trefiak WD, Desser SS (1973) Crystalloid inclusions in species of Leucocytozoon, Parahaemoproteus, and Plasmodium. J Protozool 20(1):73–80
Tsaousis AD, Kunji ER, Goldberg AV et al (2008) A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453(7194):553–556. https://doi.org/10.1038/nature06903
Tsaousis AD, Gaston D, Stechmann A et al (2011) A functional Tom70 in the human parasite Blastocystis sp.: implications for the evolution of the mitochondrial import apparatus. Mol Biol Evol 28(1):781–791. https://doi.org/10.1093/molbev/msq252
Uni S, Iseki M, Maekawa T et al (1987) Ultrastructure of Cryptosporidium muris (strain RN 66) parasitizing the murine stomach. Parasitol Res 74(2):123–132
van der Giezen M (2005) Endosymbiosis: past and present. Heredity
van der Giezen M, Tovar J (2005) Degenerate mitochondria. EMBO Rep 6(6):525–530
van der Giezen M, Tovar J, Clark CG (2005) Mitochondrion-derived organelles in protists and fungi. Int Rev Cytol 244:175–225. https://doi.org/10.1016/S0074-7696(05)44005-X
van Dooren GG, Marti M, Tonkin CJ et al (2005) Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum. Mol Microbiol 57(2):405–419. https://doi.org/10.1111/j.1365-2958.2005.04699.x
van Hoek AH, Akhmanova AS, Huynen MA et al (2000) A mitochondrial ancestry of the hydrogenosomes of Nyctotherus ovalis. Mol Biol Evol 17(1):202–206. https://doi.org/10.1093/oxfordjournals.molbev.a026234
Vinayak S, Pawlowic MC, Sateriale A et al (2015) Genetic modification of the diarrhoeal pathogen Cryptosporidium parvum. Nature 523(7561):477–480. https://doi.org/10.1038/nature14651
Waller RF, Jabbour C, Chan NC et al (2009) Evidence of a reduced and modified mitochondrial protein import apparatus in microsporidian mitosomes. Eukaryot Cell 8(1):19–26. https://doi.org/10.1128/EC.00313-08
Wiedemann N, Pfanner N (2017) Mitochondrial machineries for protein import and assembly. Annu Rev Biochem 86:685–714. https://doi.org/10.1146/annurev-biochem-060815-014352
Williams BA, Keeling PJ (2003) Cryptic organelles in parasitic protists and fungi. Adv Parasitol 54:9–68
Williams BA, Hirt RP, Lucocq JM et al (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418(6900):865–869
Xu P, Widmer G, Wang Y et al (2004) The genome of Cryptosporidium hominis. Nature 431(7012):1107–1112. https://doi.org/10.1038/nature02977
Zhu G (2004) Current progress in the fatty acid metabolism in Cryptosporidium parvum. J Eukaryot Microbiol 51(4):381–388
Zhu G, LaGier MJ, Stejskal F et al (2002) Cryptosporidium parvum: the first protist known to encode a putative polyketide synthase. Gene 298(1):79–89. https://doi.org/10.1016/S0378-1119(02)00931-9
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This research was supported by BBSRC research grant (BB/M009971/1) to ADT. We would like to thank Miklos Müller for proofreading the manuscript and his constructive comments.
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Tsaousis, A.D., Keithly, J.S. (2019). The Mitochondrion-Related Organelles of Cryptosporidium Species. In: Tachezy, J. (eds) Hydrogenosomes and Mitosomes: Mitochondria of Anaerobic Eukaryotes. Microbiology Monographs, vol 9. Springer, Cham. https://doi.org/10.1007/978-3-030-17941-0_10
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