The Mitochondrion-Related Organelles of Cryptosporidium Species

  • Anastasios D. TsaousisEmail author
  • Janet S. Keithly
Part of the Microbiology Monographs book series (MICROMONO, volume 9)


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.



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.


  1. Abrahamsen MS (2001) Cryptosporidium parvum genome project. Comp Funct Genomics 2(1):19–21. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abrahamsen MS, Templeton TJ, Enomoto S et al (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304(5669):441–445. CrossRefPubMedGoogle Scholar
  3. 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–84SPubMedGoogle Scholar
  4. 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. CrossRefPubMedGoogle Scholar
  5. 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. CrossRefPubMedGoogle Scholar
  6. 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. CrossRefGoogle Scholar
  7. Boxma B, de Graaf RM, van der Staay GW et al (2005) An anaerobic mitochondrion that produces hydrogen. Nature 434(7029):74–79CrossRefGoogle Scholar
  8. Braymer JJ, Lill R (2017) Iron-sulfur cluster biogenesis and trafficking in mitochondria. J Biol Chem 292(31):12754–12763. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Brown JR, Doolittle WF (1997) Archaea and the prokaryote-to-eukaryote transition. Microbiol Mol Biol Rev 61(4):456–502PubMedPubMedCentralGoogle Scholar
  10. Cai X, Fuller AL, McDougald LR et al (2003) Apicoplast genome of the coccidian Eimeria tenella. Gene 321:39–46. CrossRefPubMedGoogle Scholar
  11. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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. CrossRefPubMedGoogle Scholar
  13. 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):737–742CrossRefGoogle Scholar
  14. Clark CG, Roger AJ (1995) Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc Natl Acad Sci U S A 92(14):6518–6521CrossRefGoogle Scholar
  15. 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 154–169CrossRefGoogle Scholar
  16. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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. CrossRefPubMedGoogle Scholar
  18. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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. CrossRefPubMedGoogle Scholar
  20. Desportes I, Schrével J (2013) Treatise on zoology - anatomy, taxonomy, biology. The gregarines. The early branching Apicomplexa. BRILL, LeidenGoogle Scholar
  21. 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):10924–10929CrossRefGoogle Scholar
  22. Dolezal P, Likic V, Tachezy J et al (2006) Evolution of the molecular machines for protein import into mitochondria. Science 313(5785):314–318CrossRefGoogle Scholar
  23. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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. CrossRefPubMedGoogle Scholar
  25. 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. CrossRefGoogle Scholar
  26. Entrala E, Mascaro C (1997) Glycolytic enzyme activities in Cryptosporidium parvum oocysts. FEMS Microbiol Lett 151(1):51–57. CrossRefPubMedGoogle Scholar
  27. Fayer R, Xiao L (2007) Cryptosporidium and cryptosporidiosis. CRC PressGoogle Scholar
  28. Fenchel T, Perry T, Thane A (1977) Anaerobiosis and symbiosis with bacteria in free-living ciliates. J Protozool 24(1):154–163CrossRefGoogle Scholar
  29. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Frey TG, Perkins GA, Ellisman MH (2006) Electron tomography of membrane-bound cellular organelles. Annu Rev Biophys Biomol Struct 35:199–224. CrossRefPubMedGoogle Scholar
  31. Fry M, Beesley JE (1991) Mitochondria of mammalian Plasmodium spp. Parasitology 102(Pt 1):17–26CrossRefGoogle Scholar
  32. 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):1149–1160CrossRefGoogle Scholar
  33. Goldberg AV, Molik S, Tsaousis AD et al (2008) Localization and functionality of microsporidian iron-Sulphur cluster assembly proteins. Nature 452(7187):624–628. CrossRefPubMedGoogle Scholar
  34. 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. CrossRefPubMedGoogle Scholar
  35. Henriquez FL, Richards TA, Roberts F et al (2005) The unusual mitochondrial compartment of Cryptosporidium parvum. Trends Parasitol 21(2):68–74. CrossRefPubMedGoogle Scholar
  36. Horner DS, Foster PG, Embley TM (2000) Iron hydrogenases and the evolution of anaerobic eukaryotes. Mol Biol Evol 17(11):1695–1709CrossRefGoogle Scholar
  37. Inui H, Ono K, Miyatake K et al (1987) Purification and characterization of pyruvate:NADP+ oxidoreductase in Euglena gracilis. J Biol Chem 262(19):9130–9135PubMedGoogle Scholar
  38. Jerlstrom-Hultqvist J, Einarsson E, Xu F et al (2013) Hydrogenosomes in the diplomonad Spironucleus salmonicida. Nat Commun 4:2493. CrossRefPubMedPubMedCentralGoogle Scholar
  39. 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. CrossRefPubMedGoogle Scholar
  40. Katinka MD, Duprat S, Cornillot E et al (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414(6862):450–453CrossRefGoogle Scholar
  41. 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):975–980CrossRefGoogle Scholar
  42. Keeling PJ (2004) Reduction and compaction in the genome of the apicomplexan parasite Cryptosporidium parvum. Dev Cell 6(5):614–616. CrossRefPubMedGoogle Scholar
  43. Keeling PJ, Fast NM (2002) Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu Rev Microbiol 56:93–116CrossRefGoogle Scholar
  44. 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. CrossRefPubMedGoogle Scholar
  45. 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. CrossRefPubMedGoogle Scholar
  46. 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):636–642PubMedGoogle Scholar
  47. Krungkrai J, Prapunwattana P, Krungkrai SR (2000) Ultrastructure and function of mitochondria in gametocytic stage of Plasmodium falciparum. Parasite 7(1):19–26. CrossRefPubMedGoogle Scholar
  48. 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. CrossRefPubMedGoogle Scholar
  49. 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. CrossRefGoogle Scholar
  50. 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):1245–1250CrossRefGoogle Scholar
  51. 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. CrossRefPubMedGoogle Scholar
  52. 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. CrossRefGoogle Scholar
  53. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lucic V, Forster F, Baumeister W (2005) Structural studies by electron tomography: from cells to molecules. Annu Rev Biochem 74:833–865. CrossRefPubMedGoogle Scholar
  55. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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. CrossRefGoogle Scholar
  57. 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. CrossRefPubMedGoogle Scholar
  58. Mannella CA (2006) The relevance of mitochondrial membrane topology to mitochondrial function. Biochim Biophys Acta 1762(2):140–147. CrossRefPubMedGoogle Scholar
  59. 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. CrossRefPubMedGoogle Scholar
  60. 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. CrossRefPubMedGoogle Scholar
  61. Mauzy MJ, Enomoto S, Lancto CA et al (2012) The Cryptosporidium parvum transcriptome during in vitro development. PLoS One 7(3):e31715. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Melo EJ, Attias M, De Souza W (2000) The single mitochondrion of tachyzoites of Toxoplasma gondii. J Struct Biol 130(1):27–33. CrossRefPubMedGoogle Scholar
  63. Mi-Ichi F, Takeo S, Takashima E et al (2003) Unique properties of respiratory chain in Plasmodium falciparum mitochondria. Adv Exp Med Biol 531:117–133CrossRefGoogle Scholar
  64. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  65. Miller CN, Josse L, Tsaousis AD (2018b) Localization of Fe-S biosynthesis machinery in Cryptosporidium parvum Mitosome. J Eukaryot Microbiol 65:913. CrossRefPubMedPubMedCentralGoogle Scholar
  66. Mogi T, Kita K (2010) Diversity in mitochondrial metabolic pathways in parasitic protists Plasmodium and Cryptosporidium. Parasitol Int 59(3):305–312. CrossRefPubMedGoogle Scholar
  67. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  68. Nakazawa M, Inui H, Yamaji R et al (2000) The origin of pyruvate: NADP+ oxidoreductase in mitochondria of Euglena gracilis. FEBS Lett 479(3):155–156CrossRefGoogle Scholar
  69. Nasirudeen AM, Tan KS (2004) Isolation and characterization of the mitochondrion-like organelle from Blastocystis hominis. J Microbiol Methods 58(1):101–109CrossRefGoogle Scholar
  70. Ovciarikova J, Lemgruber L, Stilger KL et al (2017) Mitochondrial behaviour throughout the lytic cycle of Toxoplasma gondii. Sci Rep 7:42746. CrossRefPubMedPubMedCentralGoogle Scholar
  71. 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. CrossRefPubMedGoogle Scholar
  72. Petry F, Harris JR (1999) Ultrastructure, fractionation and biochemical analysis of Cryptosporidium parvum sporozoites. Int J Parasitol 29(8):1249–1260. CrossRefPubMedGoogle Scholar
  73. Putignani L, Tait A, Smith HV et al (2004) Characterization of a mitochondrion-like organelle in Cryptosporidium parvum. Parasitology 129(Pt 1):1–18CrossRefGoogle Scholar
  74. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  75. 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–55SPubMedGoogle Scholar
  76. Riordan CE, Ault JG, Langreth SG et al (2003) Cryptosporidium parvum Cpn60 targets a relict organelle. Curr Genet 44(3):138–147. CrossRefPubMedGoogle Scholar
  77. 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. CrossRefPubMedGoogle Scholar
  78. 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. CrossRefPubMedGoogle Scholar
  79. 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. CrossRefPubMedGoogle Scholar
  80. 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. CrossRefPubMedGoogle Scholar
  81. 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. CrossRefPubMedGoogle Scholar
  82. 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. CrossRefGoogle Scholar
  83. Slapeta J, Keithly JS (2004) Cryptosporidium parvum mitochondrial-type HSP70 targets homologous and heterologous mitochondria. Eukaryot Cell 3(2):483–494CrossRefGoogle Scholar
  84. 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. CrossRefPubMedGoogle Scholar
  85. 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. CrossRefPubMedGoogle Scholar
  86. Tan KS (2008) New insights on classification, identification, and clinical relevance of Blastocystis spp. Clin Microbiol Rev 21(4):639–665. CrossRefPubMedPubMedCentralGoogle Scholar
  87. Templeton TJ, Iyer LM, Anantharaman V et al (2004) Comparative analysis of apicomplexa and genomic diversity in eukaryotes. Genome Res 14(9):1686–1695. CrossRefPubMedPubMedCentralGoogle Scholar
  88. 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. CrossRefPubMedGoogle Scholar
  89. 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. CrossRefPubMedGoogle Scholar
  90. Thompson RC, Olson ME, Zhu G et al (2005) Cryptosporidium and cryptosporidiosis. Adv Parasitol 59:77–158CrossRefGoogle Scholar
  91. 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):1013–1021CrossRefGoogle Scholar
  92. Tovar J, Leon-Avila G, Sanchez LB et al (2003) Mitochondrial remnant organelles of Giardia function in iron-Sulphur protein maturation. Nature 426(6963):172–176CrossRefGoogle Scholar
  93. Trefiak WD, Desser SS (1973) Crystalloid inclusions in species of Leucocytozoon, Parahaemoproteus, and Plasmodium. J Protozool 20(1):73–80CrossRefGoogle Scholar
  94. 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. CrossRefPubMedGoogle Scholar
  95. 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. CrossRefPubMedGoogle Scholar
  96. Uni S, Iseki M, Maekawa T et al (1987) Ultrastructure of Cryptosporidium muris (strain RN 66) parasitizing the murine stomach. Parasitol Res 74(2):123–132CrossRefGoogle Scholar
  97. van der Giezen M (2005) Endosymbiosis: past and present. HeredityGoogle Scholar
  98. van der Giezen M, Tovar J (2005) Degenerate mitochondria. EMBO Rep 6(6):525–530CrossRefGoogle Scholar
  99. van der Giezen M, Tovar J, Clark CG (2005) Mitochondrion-derived organelles in protists and fungi. Int Rev Cytol 244:175–225. CrossRefPubMedGoogle Scholar
  100. 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. CrossRefPubMedGoogle Scholar
  101. 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. CrossRefGoogle Scholar
  102. Vinayak S, Pawlowic MC, Sateriale A et al (2015) Genetic modification of the diarrhoeal pathogen Cryptosporidium parvum. Nature 523(7561):477–480. CrossRefPubMedPubMedCentralGoogle Scholar
  103. 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. CrossRefPubMedGoogle Scholar
  104. Wiedemann N, Pfanner N (2017) Mitochondrial machineries for protein import and assembly. Annu Rev Biochem 86:685–714. CrossRefPubMedGoogle Scholar
  105. Williams BA, Keeling PJ (2003) Cryptic organelles in parasitic protists and fungi. Adv Parasitol 54:9–68CrossRefGoogle Scholar
  106. Williams BA, Hirt RP, Lucocq JM et al (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418(6900):865–869CrossRefGoogle Scholar
  107. Xu P, Widmer G, Wang Y et al (2004) The genome of Cryptosporidium hominis. Nature 431(7012):1107–1112. CrossRefPubMedGoogle Scholar
  108. Zhu G (2004) Current progress in the fatty acid metabolism in Cryptosporidium parvum. J Eukaryot Microbiol 51(4):381–388CrossRefGoogle Scholar
  109. 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. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Laboratory for Evolutionary and Molecular Parasitology, RAPID GroupSchool of Biosciences, University of KentCanterbury, KentUK
  2. 2.Division of Infectious Diseases/Office of Research and Technology, New York State Department of HealthThe Wadsworth CenterAlbanyUSA
  3. 3.Department of Biomedical SciencesSchool of Public Health, SUNY-AlbanyAlbanyUSA

Personalised recommendations