Advertisement

The Mitochondrion-Related Organelles of Blastocystis

  • Anastasios D. TsaousisEmail author
  • Nigel Yarlett
  • Kevin S. W. Tan
Chapter
Part of the Microbiology Monographs book series (MICROMONO, volume 9)

Abstract

Blastocystis is an anaerobic microbial eukaryote that inhabits the gut of various animals. While it was considered to be a parasite, its pathogenicity is controversial, since recent estimations suggest that Blastocystis could be present in more than one billion humans. Blastocystis belongs to the stramenopiles (heterokonts), a diverse group of eukaryotes that also include unicellular diatoms and giant multicellular kelps. The Blastocystis cell lacks typical features of other stramenopiles; its genome has laterally acquired many genes from other prokaryotes and eukaryotes, resulting in having exceptional biochemistry and unique adaptations of its mitochondria. For example, Blastocystis mitochondrion-related organelles (MROs) have characteristics of typical mitochondria, including Complexes I and II from electron transport chain, mitochondrial DNA, Fe-S cluster assembly and amino acid metabolism, but also proteins that are typically present in obligate anaerobes including FeFe-hydrogenase, pyruvate metabolism and alternative oxidase. Some of the pathways have been localized and biochemically characterized, providing a better understanding on the functions of these organelles. In this chapter, we will present and examine the status quo regarding the biology and morphology of Blastocystis MROs, and we will discuss future avenues on exploring even further adaptations of these organelles.

Notes

Acknowledgements

Dr. Anastasios D. Tsaousis’ research on Blastocystis mitochondria was supported by BBSRC research grant (BB/M009971/1).

References

  1. Abrahamian M, Kagda M, Ah-Fong AMV et al (2017) Rethinking the evolution of eukaryotic metabolism: novel cellular partitioning of enzymes in stramenopiles links serine biosynthesis to glycolysis in mitochondria. BMC Evol Biol 17(1):241.  https://doi.org/10.1186/s12862-017-1087-8 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Akhmanova A, Voncken F, van Alen T et al (1998) A hydrogenosome with a genome. Nature 396(6711):527–528CrossRefGoogle Scholar
  3. Andersen LO, Stensvold CR (2016) Blastocystis in health and disease: are we moving from a clinical to a public health perspective? J Clin Microbiol 54(3):524–528.  https://doi.org/10.1128/JCM.02520-15 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Betts EL, Gentekaki E, Thomasz A et al (2018) Genetic diversity of Blastocystis in non-primate animals. Parasitology 145:1–7.  https://doi.org/10.1017/S0031182017002347 CrossRefGoogle Scholar
  5. Boreham PF, Stenzel DJ (1993) The current status of Blastocystis hominis. Parasitol Today 9(7):251CrossRefGoogle Scholar
  6. Bruderer T, Wehrli C, Kohler P (1996) Cloning and characterization of the gene encoding pyruvate phosphate dikinase from Giardia duodenalis. Mol Biochem Parasitol 77(2):225–233CrossRefGoogle Scholar
  7. Bui ET, Bradley PJ, Johnson PJ (1996) A common evolutionary origin for mitochondria and hydrogenosomes. Proc Natl Acad Sci USA 93(18):9651–9656CrossRefGoogle Scholar
  8. Cavalier-Smith T (1987) Eukaryotes with no mitochondria. Nature 326(6111):332–333CrossRefGoogle Scholar
  9. Chan NC, Likic VA, Waller RF et al (2006) The C-terminal TPR domain of Tom70 defines a family of mitochondrial protein import receptors found only in animals and fungi. J Mol Biol 358(4):1010–1022.  https://doi.org/10.1016/j.jmb.2006.02.062 CrossRefPubMedGoogle Scholar
  10. Clark CG (1997) Extensive genetic diversity in Blastocystis hominis. Mol Biochem Parasitol 87(1):79–83.  https://doi.org/10.1016/S0166-6851(97)00046-7 CrossRefPubMedGoogle Scholar
  11. Clark CG, van der Giezen M, Alfellani MA et al (2013) Recent developments in Blastocystis research. Adv Parasitol 82:1–32.  https://doi.org/10.1016/B978-0-12-407706-5.00001-0 CrossRefPubMedGoogle Scholar
  12. Dacks JB, Dyal PL, Embley TM et al (2006) Hydrogenosomal succinyl-CoA synthetase from the rumen-dwelling fungus Neocallimastix patriciarum; an energy-producing enzyme of mitochondrial origin. Gene 373:75–82.  https://doi.org/10.1016/j.gene.2006.01.012 CrossRefPubMedGoogle Scholar
  13. Denoeud F, Roussel M, Noel B et al (2011) Genome sequence of the stramenopile Blastocystis, a human anaerobic parasite. Genome Biol 12(3):R29.  https://doi.org/10.1186/gb-2011-12-3-r29 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Deramchia K, Morand P, Biran M et al (2014) Contribution of pyruvate phosphate dikinase in the maintenance of the glycosomal ATP/ADP balance in the Trypanosoma brucei procyclic form. J Biol Chem 289(25):17365–17378.  https://doi.org/10.1074/jbc.M114.567230 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Dhurga DB, Suresh K, Tan TC (2016) Granular formation during apoptosis in Blastocystis sp. exposed to metronidazole (MTZ). PLoS One 11(7):e0155390.  https://doi.org/10.1371/journal.pone.0155390 CrossRefPubMedPubMedCentralGoogle Scholar
  16. DosReis GA, Barcinski MA (2001) Apoptosis and parasitism: from the parasite to the host immune response. Adv Parasitol 49:133–161CrossRefGoogle Scholar
  17. Dunn LA, Boreham PF, Stenzel DJ (1989) Ultrastructural variation of Blastocystis hominis stocks in culture. Int J Parasitol 19(1):43–56.  https://doi.org/10.1016/0020-7519(89)90020-9 CrossRefPubMedGoogle Scholar
  18. Dyall SD, Koehler CM, Delgadillo-Correa MG et al (2000) Presence of a member of the mitochondrial carrier family in hydrogenosomes: conservation of membrane-targeting pathways between hydrogenosomes and mitochondria. Mol Cell Biol 20(7):2488–2497CrossRefGoogle Scholar
  19. Embley TM, van der Giezen M, Horner DS et al (2003) Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55(7):387–395CrossRefGoogle Scholar
  20. Eme L, Gentekaki E, Curtis B et al (2017) Lateral gene transfer in the adaptation of the anaerobic parasite Blastocystis to the gut. Curr Biol 27(6):807–820.  https://doi.org/10.1016/j.cub.2017.02.003 CrossRefPubMedGoogle Scholar
  21. Gentekaki E, Curtis BA, Stairs CW et al (2017) Extreme genome diversity in the hyper-prevalent parasitic eukaryote Blastocystis. PLoS Biol 15(9):e2003769.  https://doi.org/10.1371/journal.pbio.2003769 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Giege P, Heazlewood JL, Roessner-Tunali U et al (2003) Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 15(9):2140–2151CrossRefGoogle Scholar
  23. Goyeneche AA, Harmon JM, Telleria CM (2006) Cell death induced by serum deprivation in luteal cells involves the intrinsic pathway of apoptosis. Reproduction 131(1):103–111.  https://doi.org/10.1530/rep.1.00751 CrossRefPubMedGoogle Scholar
  24. Graham JW, Williams TC, Morgan M et al (2007) Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell 19(11):3723–3738.  https://doi.org/10.1105/tpc.107.053371 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gray MW, Burger G, Lang BF (2001) The origin and early evolution of mitochondria. Genome Biol 2(6).  https://doi.org/10.1186/gb-2001-2-6-reviews1018 CrossRefGoogle Scholar
  26. Hamblin K, Standley DM, Rogers MB et al (2008) Localization and nucleotide specificity of Blastocystis succinyl-CoA synthetase. Mol Microbiol 68(6):1395–1405.  https://doi.org/10.1111/j.1365-2958.2008.06228.x CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hrdy I, Hirt RP, Dolezal P et al (2004) Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432(7017):618–622CrossRefGoogle Scholar
  28. 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
  29. Jacob AS, Andersen LO, Bitar PP et al (2016) Blastocystis mitochondrial genomes appear to show multiple independent gains and losses of start and stop codons. Genome Biol Evol 8(11):3340–3350.  https://doi.org/10.1093/gbe/evw255 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kamikawa R, Moog D, Zauner S et al (2017) A non-photosynthetic diatom reveals early steps of reductive evolution in plastids. Mol Biol Evol 34(9):2355–2366.  https://doi.org/10.1093/molbev/msx172 CrossRefPubMedGoogle Scholar
  31. 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 CrossRefPubMedGoogle Scholar
  32. Kurland CG, Andersson SG (2000) Origin and evolution of the mitochondrial proteome. Microbiol Mol Biol Rev 64(4):786–820CrossRefGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. Lavier G (1952) Blastocystis spp. Ann Parasitol Hum Comp 27(1–3):339–356CrossRefGoogle Scholar
  35. Leger MM, Eme L, Hug LA et al (2016) Novel Hydrogenosomes in the microaerophilic Jakobid Stygiella incarcerata. Mol Biol Evol 33(9):2318–2336.  https://doi.org/10.1093/molbev/msw103 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Liaud MF, Lichtle C, Apt K et al (2000) Compartment-specific isoforms of TPI and GAPDH are imported into diatom mitochondria as a fusion protein: evidence in favor of a mitochondrial origin of the eukaryotic glycolytic pathway. Mol Biol Evol 17(2):213–223.  https://doi.org/10.1093/oxfordjournals.molbev.a026301 CrossRefPubMedGoogle Scholar
  37. Lill R, Diekert K, Kaut A et al (1999) The essential role of mitochondria in the biogenesis of cellular iron-sulfur proteins. Biol Chem 380(10):1157–1166CrossRefGoogle Scholar
  38. Lindmark DG, Muller M (1973) Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J Biol Chem 248(22):7724–7728Google Scholar
  39. Long S, Changmai P, Tsaousis AD et al (2011) Stage-specific requirement for Isa1 and Isa2 proteins in the mitochondrion of Trypanosoma brucei and heterologous rescue by human and Blastocystis orthologues. Mol Microbiol 81(6):1403–1418.  https://doi.org/10.1111/j.1365-2958.2011.07769.x CrossRefPubMedGoogle Scholar
  40. Matsumoto Y, Yamada M, Yoshida Y (1987) Light-microscopical appearance and ultrastructure of Blastocystis hominis, an intestinal parasite of man. Zentralbl Bakteriol Mikrobiol Hyg A 264(3–4):379–385PubMedGoogle Scholar
  41. Moore AL, Albury MS (2008) Further insights into the structure of the alternative oxidase: from plants to parasites. Biochem Soc Trans 36.(Pt 5:1022–1026.  https://doi.org/10.1042/BST0361022 CrossRefPubMedGoogle Scholar
  42. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Nakayama T, Ishida K, Archibald JM (2012) Broad distribution of TPI-GAPDH fusion proteins among eukaryotes: evidence for glycolytic reactions in the mitochondrion? PLoS One 7(12):e52340.  https://doi.org/10.1371/journal.pone.0052340 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Nasirudeen AM, Tan KS (2004a) Caspase-3-like protease influences but is not essential for DNA fragmentation in Blastocystis undergoing apoptosis. Eur J Cell Biol 83(9):477–482.  https://doi.org/10.1078/0171-9335-00411 CrossRefPubMedGoogle Scholar
  45. Nasirudeen AM, Tan KS (2004b) Isolation and characterization of the mitochondrion-like organelle from Blastocystis hominis. J Microbiol Methods 58(1):101–109.  https://doi.org/10.1016/j.mimet.2004.03.008 CrossRefPubMedGoogle Scholar
  46. Nasirudeen AM, Tan KS (2005) Programmed cell death in Blastocystis hominis occurs independently of caspase and mitochondrial pathways. Biochimie 87(6):489–497.  https://doi.org/10.1016/j.biochi.2005.03.003 CrossRefPubMedGoogle Scholar
  47. Nasirudeen AM, Tan KS, Singh M et al (2001) Programmed cell death in a human intestinal parasite, Blastocystis hominis. Parasitology 123(Pt 3):235–246CrossRefGoogle Scholar
  48. Pakandl M (1999) Blastocystis sp. from pigs: ultrastructural changes occurring during polyxenic cultivation in Iscove's modified Dulbecco's medium. Parasitol Res 85(8–9):743–748CrossRefGoogle Scholar
  49. Perez-Brocal V, Clark CG (2008) Analysis of two genomes from the mitochondrion-like organelle of the intestinal parasite Blastocystis: complete sequences, gene content, and genome organization. Mol Biol Evol 25(11):2475–2482.  https://doi.org/10.1093/molbev/msn193 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Perez-Brocal V, Shahar-Golan R, Clark CG (2010) A linear molecule with two large inverted repeats: the mitochondrial genome of the stramenopile Proteromonas lacertae. Genome Biol Evol 2:257–266.  https://doi.org/10.1093/gbe/evq015 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Plaxton WC (1996) The organization and regulation of plant glycolysis. Annu Rev Plant Physiol Plant Mol Biol 47:185–214.  https://doi.org/10.1146/annurev.arplant.47.1.185 CrossRefPubMedGoogle Scholar
  52. Raman K, Kumar S, Chye TT (2016) Increase number of mitochondrion-like organelle in symptomatic Blastocystis subtype 3 due to metronidazole treatment. Parasitol Res 115(1):391–396.  https://doi.org/10.1007/s00436-015-4760-0 CrossRefPubMedGoogle Scholar
  53. Río Bártulos C, Rogers MB, Williams TA et al (2018) Mitochondrial targeting of glycolysis in a major lineage of eukaryotes. bioRxiv.  https://doi.org/10.1101/257790
  54. Rodriguez-Contreras D, Hamilton N (2014) Gluconeogenesis in Leishmania mexicana: contribution of glycerol kinase, phosphoenolpyruvate carboxykinase, and pyruvate phosphate dikinase. J Biol Chem 289(47):32989–33000.  https://doi.org/10.1074/jbc.M114.569434 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Saavedra-Lira E, Ramirez-Silva L, Perez-Montfort R (1998) Expression and characterization of recombinant pyruvate phosphate dikinase from Entamoeba histolytica. Biochim Biophys Acta 1382(1):47–54.  https://doi.org/10.1016/S0167-4838(97)00139-8 CrossRefPubMedGoogle Scholar
  56. Silard R, Panaitescu D, Burghelea B (1983) Ultrastructural aspects of Blastocystis hominis. Arch Roum Pathol Exp Microbiol 42(2–3):233–242PubMedGoogle Scholar
  57. Silberman JD, Sogin ML, Leipe DD et al (1996) Human parasite finds taxonomic home. Nature 380(6573):398.  https://doi.org/10.1038/380398a0 CrossRefPubMedGoogle Scholar
  58. Slamovits CH, Keeling PJ (2006) Pyruvate-phosphate dikinase of oxymonads and parabasalia and the evolution of pyrophosphate-dependent glycolysis in anaerobic eukaryotes. Eukaryot Cell 5(1):148–154.  https://doi.org/10.1128/EC.5.1.148-154.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 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(11):1176–1186.  https://doi.org/10.1016/j.cub.2014.04.033 CrossRefPubMedGoogle Scholar
  60. Stechmann A, Hamblin K, Perez-Brocal V et al (2008) Organelles in Blastocystis that blur the distinction between mitochondria and hydrogenosomes. Curr Biol 18(8):580–585.  https://doi.org/10.1016/j.cub.2008.03.037 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Stensvold CR (2013) Blastocystis: genetic diversity and molecular methods for diagnosis and epidemiology. Trop Parasitol 3(1):26–34.  https://doi.org/10.4103/2229-5070.113896 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Stensvold CR, Clark CG (2016) Current status of Blastocystis: a personal view. Parasitol Int 65(6 Pt B):763–771.  https://doi.org/10.1016/j.parint.2016.05.015 CrossRefPubMedGoogle Scholar
  63. Stenzel DJ, Boreham PF (1996) Blastocystis hominis revisited. Clin Microbiol Rev 9(4):563–584CrossRefGoogle Scholar
  64. Stenzel DJ, Boreham PF, McDougall R (1991) Ultrastructure of Blastocystis hominis in human stool samples. Int J Parasitol 21(7):807–812.  https://doi.org/10.1016/0020-7519(91)90149-2 CrossRefPubMedGoogle Scholar
  65. Stenzel DJ, Cassidy MF, Boreham PF (1994) Morphology of Blastocystis sp. from domestic birds. Parasitol Res 80(2):131–137CrossRefGoogle Scholar
  66. Tachezy J, Sanchez LB, Muller M (2001) Mitochondrial type iron-sulfur cluster assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis, as indicated by the phylogeny of IscS. Mol Biol Evol 18(10):1919–1928.  https://doi.org/10.1093/oxfordjournals.molbev.a003732 CrossRefPubMedGoogle Scholar
  67. Tan KS, Nasirudeen AM (2005) Protozoan programmed cell death--insights from Blastocystis deathstyles. Trends Parasitol 21(12):547–550.  https://doi.org/10.1016/j.pt.2005.09.006 CrossRefPubMedGoogle Scholar
  68. Tan KS, Howe J, Yap EH et al (2001) Do Blastocystis hominis colony forms undergo programmed cell death? Parasitol Res 87(5):362–367CrossRefGoogle Scholar
  69. Tjaden J, Haferkamp I, Boxma B et al (2004) A divergent ADP/ATP carrier in the hydrogenosomes of Trichomonas gallinae argues for an independent origin of these organelles. Mol Microbiol 51(5):1439–1446CrossRefGoogle Scholar
  70. 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
  71. 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
  72. 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 CrossRefPubMedGoogle Scholar
  73. 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 CrossRefPubMedGoogle Scholar
  74. Tsaousis AD, Ollagnier de Choudens S, Gentekaki E et al (2012) Evolution of Fe/S cluster biogenesis in the anaerobic parasite Blastocystis. Proc Natl Acad Sci U S A 109(26):10426–10431.  https://doi.org/10.1073/pnas.1116067109 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Tsaousis AD, Gentekaki E, Eme L et al (2014) Evolution of the cytosolic iron-sulfur cluster assembly machinery in Blastocystis species and other microbial eukaryotes. Eukaryot Cell 13(1):143–153.  https://doi.org/10.1128/EC.00158-13 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Tsaousis AD, Hamblin K, Elliot CR et al (2018) The human gut colonizer Blastocystis respires using complex II and alternative oxidase to buffer transient oxygen fluctuations in the gut. Front Cell Infect Microbiol 8:371CrossRefGoogle Scholar
  77. Wawrzyniak I, Courtine D, Osman M et al (2015) Draft genome sequence of the intestinal parasite Blastocystis subtype 4-isolate WR1. Genom Data 4:22–23.  https://doi.org/10.1016/j.gdata.2015.01.009 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 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 CrossRefPubMedGoogle Scholar
  79. Williams BA, Hirt RP, Lucocq JM et al (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418(6900):865–869CrossRefGoogle Scholar
  80. Yarlett N, Hann AC, Lloyd D et al (1981) Hydrogenosomes in the rumen protozoon Dasytricha ruminantium Schuberg. Biochem J 200(2):365–372CrossRefGoogle Scholar
  81. Yarlett N, Orpin CG, Munn EA et al (1986) Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. Biochem J 236(3):729–739CrossRefGoogle Scholar
  82. Yason JA, Tan KS (2015) Seeing the whole elephant: imaging flow cytometry reveals extensive morphological diversity within Blastocystis isolates. PLoS One 10(11):e0143974.  https://doi.org/10.1371/journal.pone.0143974 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Yeo JH, Lo JC, Nissom PM et al (2006) Glutamine or glucose starvation in hybridoma cultures induces death receptor and mitochondrial apoptotic pathways. Biotechnol Lett 28(18):1445–1452.  https://doi.org/10.1007/s10529-006-9110-y CrossRefPubMedGoogle Scholar
  84. Yin J, Howe J, Tan KS (2010a) Staurosporine-induced programmed cell death in Blastocystis occurs independently of caspases and cathepsins and is augmented by calpain inhibition. Microbiology 156(Pt 5):1284–1293.  https://doi.org/10.1099/mic.0.034025-0 CrossRefPubMedGoogle Scholar
  85. Yin J, Ye AJ, Tan KS (2010b) Autophagy is involved in starvation response and cell death in Blastocystis. Microbiology 156(Pt 3):665–677.  https://doi.org/10.1099/mic.0.033944-0 CrossRefPubMedGoogle Scholar
  86. Yoshikawa H, Yamada M, Yoshida Y (1988) Freeze-fracture study of Blastocystis hominis. J Protozool 35(4):522–528CrossRefGoogle Scholar
  87. Zierdt CH (1986) Cytochrome-free mitochondria of an anaerobic protozoan--Blastocystis hominis. J Protozool 33(1):67–69CrossRefGoogle Scholar
  88. Zierdt CH, Donnolley CT, Muller J et al (1988) Biochemical and ultrastructural study of Blastocystis hominis. J Clin Microbiol 26(5):965–970PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Anastasios D. Tsaousis
    • 1
    Email author
  • Nigel Yarlett
    • 2
  • Kevin S. W. Tan
    • 3
  1. 1.Laboratory of Molecular and Evolutionary Parasitology, RAPID GroupSchool of Biosciences, University of KentCanterbury, KentUK
  2. 2.Haskins Laboratories, Department of Chemistry and Physical SciencePace UniversityNew YorkUSA
  3. 3.Laboratory of Molecular and Cellular Parasitology, Department of Microbiology and ImmunologyYong Loo Lin School of Medicine, National University of SingaporeSingaporeSingapore

Personalised recommendations