• Rodney D. AdamEmail author
Living reference work entry


The diplomonads (“two units”) are characterized by their possession of two nuclei that are similar in appearance, replication, and function. Together with the Carpediemonas-like organisms and retortamonads, the diplomonads are classified within Fornicata. Each “unit” of the diplomonad cell includes a karyomastigont that has one nucleus and (usually) four flagella, which are used for locomotion. Thus, most diplomonads have two karyomastigonts. However, the “enteromonads” present an exception in that they have a single karyomastigont per cell. The diplomonads have anaerobic metabolism and lack conventional mitochondria, so they were thought to be pre-mitochondriate organisms. However, they have subsequently been shown to have highly reduced mitochondria called mitochondrion-related organelles (MRO) that perform some of the functions of conventional mitochondria. The most studied diplomonads are the Giardia species, which are intestinal pathogens or commensals for a variety of vertebrates from amphibians to mammals and include pathogens of humans. Like Giardia spp., the Spironucleus species also replicate in the host intestine, in this case in vertebrates or invertebrates and include notable fish pathogens. In contrast, Hexamita and Trepomonas species can be either free-living or parasitic.


Mastigont Binucleate Mitosome Mitochondrion-like organelle (MRO) Anaerobic Hexamita Spironucleus Trepomonas Enteromonas Trimitus Trigonomonas Gyromonas Giardia Octomitus Brugerolleia 


  1. Abe, N., Makino, I., & Kojima, A. (2012). Molecular characterization of Giardia psittaci by multilocus sequence analysis. Infection, Genetics and Evolution, 12, 1710–1716.PubMedCrossRefGoogle Scholar
  2. Adam, R. D. (1992). Chromosome-size variation in Giardia lamblia: The role of rDNA repeats. Nucleic Acids Research, 20, 3057–3061.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Adam, R. D. (2001). Biology of Giardia lamblia. Clinical Microbiology Review, 14, 447–475.CrossRefGoogle Scholar
  4. Adam, R. D., Nash, T. E., & Wellems, T. E. (1988). The Giardia lamblia trophozoite contains sets of closely related chromosomes. Nucleic Acids Research, 16, 4555–4567.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Adam, R. D., Nigam, A., Seshadri, V., Martens, C. A., Farneth, G. A., Morrison, H. G., Nash, T. E., Porcella, S. F., & Patel, R. (2010). The Giardia lamblia vsp gene repertoire: Characteristics, genomic organization, and evolution. BMC Genomics, 11, 424.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Adam, R. D., Dahlstrom, E. W., Martens, C. A., Bruno, D. P., Barbian, K. D., Ricklefs, S. M., Hernandez, M. M., Narla, N. P., Patel, R. B., Porcella, S. F., et al. (2013). Genome sequencing of Giardia lamblia genotypes A2 and B isolates (DH and GS) and comparative analysis with the genomes of genotypes A1 and E (WB and pig). Genome Biology and Evolution, 5, 2498–2511.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Aggarwal, A., & Nash, T. E. (1988). Antigenic variation of Giardia lamblia in vivo. Infection and Immunity, 56, 1420–1423.PubMedPubMedCentralGoogle Scholar
  8. Andersson, J. O., Sjogren, A. M., Horner, D. S., Murphy, C. A., Dyal, P. L., Svard, S. G., Logsdon Jr., J. M., Ragan, M. A., Hirt, R. P., & Roger, A. J. (2007). A genomic survey of the fish parasite Spironucleus salmonicida indicates genomic plasticity among diplomonads and significant lateral gene transfer in eukaryote genome evolution. BMC Genomics, 8, 51.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bernander, R., Palm, J. E., & Svard, S. G. (2001). Genome ploidy in different stages of the Giardia lamblia life cycle. Cellular Microbiology, 3, 55–62.PubMedCrossRefGoogle Scholar
  10. Biagini, G. A., Suller, M. T., Finlay, B. J., & Lloyd, D. (1997). Oxygen uptake and antioxidant responses of the free-living diplomonad Hexamita sp. The Journal of Eukaryotic Microbiology, 44, 447–453.PubMedCrossRefGoogle Scholar
  11. Biagini, G. A., McIntyre, P. S., Finlay, B. J., & Lloyd, D. (1998). Carbohydrate and amino acid fermentation in the free-living primitive protozoon Hexamita sp. Applied and Environmental Microbiology, 64, 203–207.PubMedPubMedCentralGoogle Scholar
  12. Biagini, G. A., Yarlett, N., Ball, G. E., Billetz, A. C., Lindmark, D. G., Martinez, M. P., Lloyd, D., & Edwards, M. R. (2003). Bacterial-like energy metabolism in the amitochondriate protozoon Hexamita inflata. Molecular and Biochemical Parasitology, 128, 11–19.PubMedCrossRefGoogle Scholar
  13. Bingham, A. K., & Meyer, E. A. (1979). Giardia excystation can be induced in vitro in acidic solutions. Nature, 277, 301–302.PubMedCrossRefGoogle Scholar
  14. Birky Jr., C. W. (2010). Giardia sex? Yes, but how and how much? Trends in Parasitology, 26, 70–74.PubMedCrossRefGoogle Scholar
  15. Brugerolle, G. (1974). Contribution a l’etude cytologique et phyletique des diplozaires (Zoomastigophorea, Diplozoa, Dangered 1910): III. Etude ultrastructurale du Hexamita (Dujardin 1836). Protistologica 10, 83–90.Google Scholar
  16. Brugerolle, G. (1975). Ultrastructure of the genus Enteromonas da Fonseca (Zoomastigophorea) and revision of the order of diplomonadida Wenyon. The Journal of Protozoology, 22, 468–475.PubMedCrossRefGoogle Scholar
  17. Brugerolle, G. (1991). Flagellar and cytoskeletal systems in amitochondrial flagellates: Archamoeba, Metamonada and Parabasala. Prototplasma, 164, 70–90.Google Scholar
  18. Bui, E. T., Bradley, P. J., & Johnson, P. J. (1996). A common evolutionary origin for mitochondria and hydrogenosomes. Proceedings of the National Academy of Sciences of the United States of America, 93, 9651–9656.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Butler, G., Rasmussen, M. D., Lin, M. F., Santos, M. A., Sakthikumar, S., Munro, C. A., Rheinbay, E., Grabherr, M., Forche, A., Reedy, J. L., et al. (2009). Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature, 459, 657–662.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Caccio, S. M., & Ryan, U. (2008). Molecular epidemiology of giardiasis. Molecular and Biochemical Parasitology, 160, 75–80.PubMedCrossRefGoogle Scholar
  21. Carpenter, M. L., Assaf, Z. J., Gourguechon, S., & Cande, W. Z. (2012). Nuclear inheritance and genetic exchange without meiosis in the binucleate parasite Giardia intestinalis. Journal of Cell Science, 125, 2523–2532.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cavalier-Smith, T. (1983). A 6-kingdom classification and a unified phylogeny. In W. Schwemmler & H. E. A. Schenk (Eds.), Endocytobiology II (pp. 1027–1034). Berlin: de Gruyter.Google Scholar
  23. Cavalier-Smith, T. (2013). Early evolution of eukaryote feeding modes, cell structural diversity, and classification of the protozoan phyla Loukozoa, Sulcozoa, and Choanozoa. European Journal of Protistology, 49, 115–178.PubMedCrossRefGoogle Scholar
  24. Cavalier-Smith, T., & Chao, E. E. (1996). Molecular phylogeny of the free-living archezoan Trepomonas agilis and the nature of the first eukaryote. Journal of Molecular Evolution, 43, 551–562.PubMedCrossRefGoogle Scholar
  25. Cooper, M. A., Adam, R. D., Worobey, M., & Sterling, C. R. (2007). Population genetics provides evidence for recombination in Giardia. Current Biology, 17, 1984–1988.PubMedCrossRefGoogle Scholar
  26. Cooper, M. A., Sterling, C. R., Gilman, R. H., Cama, V., Ortega, Y., & Adam, R. D. (2010). Molecular analysis of household transmission of Giardia lamblia in a region of high endemicity in Peru. Journal of Infectious Diseases, 202, 1713–1721.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Dacks, J. B., Davis, L. A., Sjogren, A. M., Andersson, J. O., Roger, A. J., & Doolittle, W. F. (2003). Evidence for Golgi bodies in proposed ‘Golgi-lacking’ lineages. Proceedings of the Biological Sciences, 270(Suppl 2), S168–S171.CrossRefGoogle Scholar
  28. Davids, B. J., Reiner, D. S., Birkeland, S. R., Preheim, S. P., Cipriano, M. J., McArthur, A. G., & Gillin, F. D. (2006). A new family of giardial cysteine-rich non-VSP protein genes and a novel cyst protein. PLoS ONE, 1, e44.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Desser, S. S., Hong, H., & Siddall, M. E. (1993). An ultrastructural study of Brugerolleia algonquinensis gen. nov., sp. nov. (Diplomonadina; diplomonadida), a flagellate parasite in the blood of frogs from Ontario, Canada. European Journal Protistol, 29, 72–80.CrossRefGoogle Scholar
  30. Dobell, C. (1920). The discovery of the intestinal protozoa of man. Proceedings of the Royal Society of Medicine, 13, 1–15.PubMedPubMedCentralGoogle Scholar
  31. Dobell, C., & Laidlaw, P. P. (1926). On the cultivation of Entamoeba histolytica and some other entozoic amoebae. Parasitology, 18, 283–318.CrossRefGoogle Scholar
  32. Dujardin, F. (1841). Histoire naturelle des Zoophytes. Infusoires. Paris: Rowan.Google Scholar
  33. Edwards, M. R., Schofield, P. J., O’Sullivan, W. J., & Costello, M. (1992). Arginine metabolism during culture of Giardia intestinalis. Molecular and Biochemical Parasitology, 53, 97–103.PubMedCrossRefGoogle Scholar
  34. Elmendorf, H. G., Dawson, S. C., & McCaffery, J. M. (2003). The cytoskeleton of Giardia lamblia. International Journal for Parasitology, 33, 3–28.PubMedCrossRefGoogle Scholar
  35. Embley, T. M., & Martin, W. (2006). Eukaryotic evolution, changes and challenges. Nature, 440, 623–630.PubMedCrossRefGoogle Scholar
  36. Erlandsen, S. L., & Bemrick, W. J. (1987). SEM evidence for a new species, Giardia psittaci. Journal of Parasitology, 73, 623–629.PubMedCrossRefGoogle Scholar
  37. Erlandsen, S. L., Bemrick, W. J., Wells, C. L., Feely, D. E., Knudson, L., Campbell, S. R., van Keulen, H., & Jarroll, E. L. (1990). Axenic culture and characterization of Giardia ardeae from the great blue heron ( Ardea herodias ). Journal of Parasitology, 76, 717–724.PubMedCrossRefGoogle Scholar
  38. Eyden, B. P., & Vickerman, K. (1975). Ultrastructure and vacuolar movements in the free-living diplomonad Trepomonas agilis Klebs. Journal of Protozoology, 22, 54–66.CrossRefGoogle Scholar
  39. Fard, M. R., Jorgensen, A., Sterud, E., Bleiss, W., & Poynton, S. L. (2007). Ultrastructure and molecular diagnosis of Spironucleus salmonis (diplomonadida) from rainbow trout Oncorhynchus mykiss in Germany. DisAquatOrgan, 75, 37–50.Google Scholar
  40. Feely, D. E., Holberton, D. V., & Erlandsen, S. L. (1990). The biology of Giardia. In E. A. Meyer (Ed.), Giardiasis (pp. 1–49). Amsterdam: Elsevier.Google Scholar
  41. Feely, D. E., Gardner, M. D., & Hardin, E. L. (1991). Excystation of Giardia muris induced by a phosphate-bicarbonate medium: Localization of acid phosphatase. Journal of Parasitology, 77, 441–448.PubMedCrossRefGoogle Scholar
  42. Feng, X. M., Cao, L. J., Adam, R. D., Zhang, X. C., & Lu, S. Q. (2008). The catalyzing role of PPDK in Giardia lamblia. Biochemical and Biophysical Research Communications, 367, 394–398.PubMedCrossRefGoogle Scholar
  43. Filice, F. P. (1952). Studies on the cytology and life history of a Giardia from the laboratory rat. Berkeley: University of California Press.Google Scholar
  44. Forche, A., Alby, K., Schaefer, D., Johnson, A. D., Berman, J., & Bennett, R. J. (2008). The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biology, 6, e110.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Franzen, O., Jerlstrom-Hultqvist, J., Castro, E., Sherwood, E., Ankarklev, J., Reiner, D. S., Palm, D., Andersson, J. O., Andersson, B., & Svard, S. G. (2009). Draft genome sequencing of Giardia intestinalis assemblage B isolate GS: Is human giardiasis caused by two different species? PLoS Pathogens, 5, e1000560.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Ghosh, S., Frisardi, M., Rogers, R., & Samuelson, J. (2001). How Giardia swim and divide. Infection and Immunity, 69, 7866–7872.PubMedPubMedCentralCrossRefGoogle Scholar
  47. Gillin, F. D. (1987). Giardia lamblia: The role of conjugated and unconjugated bile salts in killing by human milk. Experimental Parasitology, 63, 74–83.PubMedCrossRefGoogle Scholar
  48. Gottstein, B., & Nash, T. E. (1991). Antigenic variation in Giardia lamblia: Infection of congenitally athymic nude and scid mice. Parasite Immunology, 13, 649–659.PubMedCrossRefGoogle Scholar
  49. Grassi, B. (1881). Di un nouvo parassita dell’uomo Negastoma entericum (mihi). Gazzetta dell’ Ospedale di Milano, 2, 575–580.Google Scholar
  50. Holberton, D. V. (1973). Fine structure of the ventral disk apparatus and the mechanism of attachment in the flagellate, Giardia muris. Journal of Cell Science, 13, 11–41.PubMedGoogle Scholar
  51. Holberton, D. V. (1974). Attachment of Giardia -a hydrodynamic model based on flagellar activity. The Journal of Experimental Biology, 60, 207–221.PubMedGoogle Scholar
  52. Horner, D. S., & Embley, T. M. (2001). Chaperonin 60 phylogeny provides further evidence for secondary loss of mitochondria among putative early-branching eukaryotes. Molecular Biology and Evolution, 18, 1970–1975.PubMedCrossRefGoogle Scholar
  53. Hou, G., Le Blancq, S. M., Yaping, E., Zhu, H., & Lee, M. G. (1995). Structure of a frequently rearranged rRNA-encoding chromosome in Giardia lamblia. Nucleic Acids Research, 23, 3310–3317.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hrdy, I., Mertens, E., & Nohynkova, E. (1993). Giardia intestinalis: Detection and characterization of a pyruvate phosphate dikinase. Experimental Parasitology, 76, 438–441.PubMedCrossRefGoogle Scholar
  55. Inge, P. M., Edson, C. M., & Farthing, M. J. (1988). Attachment of Giardia lamblia to rat intestinal epithelial cells. Gut, 29, 795–801.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Januschka, M. M., Erlandsen, S. L., Bemrick, W. J., Schupp, D. G., & Feely, D. E. (1988). A comparison of Giardia microti and Spironucleus muris cysts in the vole: An immunocytochemical, light, and electron microscopic study. Journal of Parasitology, 74, 452–458.PubMedCrossRefGoogle Scholar
  57. Jerlstrom-Hultqvist, J., Einarsson, E., Xu, F., Hjort, K., Ek, B., Steinhauf, D., Hultenby, K., Bergquist, J., Andersson, J. O., & Svard, S. G. (2013). Hydrogenosomes in the diplomonad Spironucleus salmonicida. Nature Communications, 4, 2493.PubMedPubMedCentralCrossRefGoogle Scholar
  58. Jirakova, K., Kulda, J., & Nohynkova, E. (2012). How nuclei of Giardia pass through cell differentiation: Semi-open mitosis followed by nuclear interconnection. Protist, 163, 465–479.PubMedCrossRefGoogle Scholar
  59. Jorgensen, A., & Sterud, E. (2006). The marine pathogenic genotype of Spironucleus barkhanus from farmed salmonids redescribed as Spironucleus salmonicida n. sp. Journal of Eukaryotic Microbiology, 53, 531–541.PubMedCrossRefGoogle Scholar
  60. Jorgensen, A., & Sterud, E. (2007). Phylogeny of Spironucleus (eopharyngia: Diplomonadida: Hexamitinae). Protist, 158, 247–254.PubMedCrossRefGoogle Scholar
  61. Kabnick, K. S., & Peattie, D. A. (1990). In situ analyses reveal that the two nuclei of Giardia lamblia are equivalent. Journal of Cell Science, 95, 353–360.PubMedGoogle Scholar
  62. Keeling, P. J., & Doolittle, W. F. (1996). A non-canonical genetic code in an early diverging eukaryotic lineage. The EMBO Journal, 15, 2285–2290.PubMedPubMedCentralGoogle Scholar
  63. Keister, D. B. (1983). Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Transactions of the Royal Society of Tropical Medicine and Hygiene, 77, 487–488.PubMedCrossRefGoogle Scholar
  64. van Keulen, H., Gutell, R. R., Gates, M. A., Campbell, S. R., Erlandsen, S. L., Jarroll, E. L., Kulda, J., & Meyer, E. A. (1993). Unique phylogenetic position of Diplomonadida based on the complete small subunit ribosomal RNA sequence of Giardia ardeae, G. muris, G. duodenalis and Hexamita sp. The FASEB Journal, 7, 223–231.PubMedGoogle Scholar
  65. van Keulen, H., Feely, D. E., Macechko, P. T., Jarroll, E. L., & Erlandsen, S. L. (1998). The sequence of Giardia small subunit rRNA shows that voles and muskrats are parasitized by a unique species Giardia microti. Journal of Parasitology, 84, 294–300.PubMedCrossRefGoogle Scholar
  66. Kolisko, M., Cepicka, I., Hampl, V., Kulda, J., & Flegr, J. (2005). The phylogenetic position of enteromonads: A challenge for the present models of diplomonad evolution. International Journal of Systematic and Evolutionary Microbiology, 55, 1729–1733.PubMedCrossRefGoogle Scholar
  67. Kolisko, M., Cepicka, I., Hampl, V., Leigh, J., Roger, A. J., Kulda, J., Simpson, A. G., & Flegr, J. (2008). Molecular phylogeny of diplomonads and enteromonads based on SSU rRNA, alpha-tubulin and HSP90 genes: Implications for the evolutionary history of the double karyomastigont of diplomonads. BMC Evolutionary Biology, 8, 205.PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kolisko, M., Silberman, J. D., Cepicka, I., Yubuki, N., Takishita, K., Yabuki, A., Leander, B. S., Inouye, I., Inagaki, Y., Roger, A. J., et al. (2010). A wide diversity of previously undetected free-living relatives of diplomonads isolated from marine/saline habitats. Environmental Microbiology, 12, 2700–2710.PubMedGoogle Scholar
  69. Kulakova, L., Singer, S. M., Conrad, J., & Nash, T. E. (2006). Epigenetic mechanisms are involved in the control of Giardia lamblia antigenic variation. Molecular Microbiology, 61, 1533–1542.PubMedCrossRefGoogle Scholar
  70. Kulda, J., & Nohynkova, E. (1978). Flagellates of the human intestine and of intestines of other species. In J. P. Kreier (Ed.), Parasitic protozoa (Vol. II, pp. 1–138). New York: Academic.Google Scholar
  71. Lambl, W. (1859). Mikroskopische untersuchungen der darmexcrete. Vierteljahrsschrift Prakstische Heikunde, 61, 1–58.Google Scholar
  72. Lanfredi-Rangel, A., Attias, M., de Carvalho, T. M., Kattenbach, W. M., & de Souza, W. (1998). The peripheral vesicles of trophozoites of the primitive protozoan Giardia lamblia May correspond to early and late endosomes and to lysosomes. Journal Structural Biology, 123, 225–235.CrossRefGoogle Scholar
  73. Lanfredi-Rangel, A., Attias, M., Reiner, D. S., Gillin, F. D., & de Souza, W. (2003). Fine structure of the biogenesis of Giardia lamblia encystation secretory vesicles. Journal of Structural Biology, 143, 153–163.PubMedCrossRefGoogle Scholar
  74. Lasek-Nesselquist, E., Welch, D. M., Thompson, R. C., Steuart, R. F., & Sogin, M. L. (2009). Genetic exchange within and between assemblages of Giardia duodenalis. Journal of Eukaryotic Microbiology, 56, 504–518.PubMedCrossRefGoogle Scholar
  75. Lasek-Nesselquist, E., Welch, D. M., & Sogin, M. L. (2010). The identification of a new Giardia duodenalis assemblage in marine vertebrates and a preliminary analysis of G. duodenalis population biology in marine systems. International Journal for Parasitology, 40, 1063–1074.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Levine, N. D., Corliss, J. O., Cox, F. E. G., Deroux, G., Grain, J., Honigberg, B. M., Leedale, G. F., Loeblich III, A. R., Lom, J., Lynn, D., et al. (1980). A newly revised classification of the protozoa. Journal of Protozoology, 27, 37–58.PubMedCrossRefGoogle Scholar
  77. Li, W., Saraiya, A. A., & Wang, C. C. (2012). The profile of snoRNA-derived microRNAs that regulate expression of variant surface proteins in Giardia lamblia. Cellular Microbiology, 14, 1455–1473.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Lindmark, D. G., & Muller, M. (1973). Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. Journal of Biological Chemistry, 248, 7724–7728.PubMedGoogle Scholar
  79. Lloyd, D., & Williams, C. F. (2014). Comparative biochemistry of Giardia, Hexamita and Spironucleus: Enigmatic diplomonads. Molecular & Biochemical Parasitology, 197, 43–49.CrossRefGoogle Scholar
  80. Lujan, H. D., Marotta, A., Mowatt, M. R., Sciaky, N., Lippincott-Schwartz, J., & Nash, T. E. (1995). Developmental induction of Golgi structure and function in the primitive eukaryote, Giardia lamblia. Journal of Biological Chemistry, 270, 4612–4618.PubMedCrossRefGoogle Scholar
  81. Lujan, H. D., Mowatt, M. R., Byrd, L. G., & Nash, T. E. (1996). Cholesterol starvation induces differentiation of the intestinal parasite Giardia lamblia. Proceedings of the National Academy of Sciences of the United States of America, 93, 7628–7633.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Martincova, E., Voleman, L., Najdrova, V., De Napoli, M., Eshar, S., Gualdron, M., Hopp, C. S., Sanin, D. E., Tembo, D. L., Van Tyne, D., et al. (2012). Live imaging of mitosomes and hydrogenosomes by HaloTag technology. PLoS One, 7, e36314.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Martincova, E., Voleman, L., Pyrih, J., Zarsky, V., Vondrackova, P., Kolisko, M., Tachezy, J., & Dolezal, P. (2015). Probing the biology of Giardia intestinalis mitosomes using in vivo enzymatic tagging. Molecular and Cellular Biology, 35, 2864–2874.PubMedPubMedCentralCrossRefGoogle Scholar
  84. Meyer, E. A. (1970). Isolation and axenic cultivation of Giardia trophozoites from the rabbit, chinchilla, and cat. Experimental Parasitology, 27, 179–183.PubMedCrossRefGoogle Scholar
  85. Meyer, E. A. (1976). Giardia lamblia: Isolation and axenic cultivation. Experimental Parasitology, 39, 101–105.PubMedCrossRefGoogle Scholar
  86. Millet, C. O., Lloyd, D., Coogan, M. P., Rumsey, J., & Cable, J. (2011a). Carbohydrate and amino acid metabolism of Spironucleus vortens. Experimental Parasitology, 129, 17–26.PubMedCrossRefGoogle Scholar
  87. Millet, C. O., Lloyd, D., Williams, C., & Cable, J. (2011b). In vitro culture of the diplomonad fish parasite Spironucleus vortens reveals unusually fast doubling time and atypical biphasic growth. Journal of Fish Diseases, 34, 71–73.PubMedCrossRefGoogle Scholar
  88. Millet, C. O., Williams, C. F., Hayes, A. J., Hann, A. C., Cable, J., & Lloyd, D. (2013). Mitochondria-derived organelles in the diplomonad fish parasite Spironucleus vortens. Experimental Parasitology, 135, 262–273.PubMedCrossRefGoogle Scholar
  89. Morrison, H. G., McArthur, A. G., Gillin, F. D., Aley, S. B., Adam, R. D., Olsen, G. J., Best, A. A., Cande, W. Z., Chen, F., Cipriano, M. J., et al. (2007). Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science, 317, 1921–1926.PubMedCrossRefGoogle Scholar
  90. Nash, T. E., & Keister, D. B. (1985). Differences in excretory-secretory products and surface antigens among 19 isolates of Giardia. Journal of Infectious Diseases, 152, 1166–1171.PubMedCrossRefGoogle Scholar
  91. Nash, T. E., McCutchan, T., Keister, D., Dame, J. B., Conrad, J. D., & Gillin, F. D. (1985). Restriction-endonuclease analysis of DNA from 15 Giardia isolates obtained from humans and animals. Journal of Infectious Diseases, 152, 64–73.PubMedCrossRefGoogle Scholar
  92. Nash, T. E., Merritt Jr., J. W., & Conrad, J. T. (1991). Isolate and epitope variability in susceptibility of Giardia lamblia to intestinal proteases. Infection and Immunity, 59, 1334–1340.PubMedPubMedCentralGoogle Scholar
  93. Nohynkova, E., Tumova, P., & Kulda, J. (2006). Cell division of Giardia intestinalis: Flagellar developmental cycle involves transformation and exchange of flagella between mastigonts of a diplomonad cell. Eukaryotic Cell, 5, 753–761.PubMedPubMedCentralCrossRefGoogle Scholar
  94. Ortega, Y. R., & Adam, R. D. (1997). Giardia: Overview and update. Clinical Infectious Diseases, 25, 545–549.PubMedCrossRefGoogle Scholar
  95. Paget, T. A., Raynor, M. H., Shipp, D. W., & Lloyd, D. (1990). Giardia lamblia produces alanine anaerobically but not in the presence of oxygen. Molecular and Biochemical Parasitology, 42, 63–67.PubMedCrossRefGoogle Scholar
  96. Perry, D. A., Morrison, H. G., & Adam, R. D. (2011). Optical map of the genotype A1 WB C6 Giardia lamblia genome isolate. Molecular and Biochemical Parasitology, 180, 112–114.PubMedPubMedCentralCrossRefGoogle Scholar
  97. Poxleitner, M. K., Carpenter, M. L., Mancuso, J. J., Wang, C. J., Dawson, S. C., & Cande, W. Z. (2008). Evidence for karyogamy and exchange of genetic material in the binucleate intestinal parasite Giardia intestinalis. Science, 319, 1530–1533.PubMedCrossRefGoogle Scholar
  98. Poynton, S. L., & Sterud, E. (2002). Guidelines for species descriptions of diplomonad flagellates from fish. Journal of Fish Diseases, 25, 15–31.CrossRefGoogle Scholar
  99. Poynton, S. L., Fraser, W., Francis-Floyd, R., Rutledge, P., Reed, P., & Nerad, T. A. (1995). Spironucleus vortens N. Sp. from the freshwater angelfish Pterophyllum scalare: Morphology and culture. Journal of Eukaryotic Microbiology, 42, 731–742.CrossRefGoogle Scholar
  100. Poynton, S. L., Fard, M. R., Jenkins, J., & Ferguson, H. W. (2004). Ultrastructure of Spironucleus salmonis n. comb. (formerly Octomitus salmonis sensu Moore 1922, Davis 1926, and Hexamita salmonis sensu Ferguson 1979), with a guide to Spironucleus species. Diseases of Aquatic Organisms, 60, 49–64.PubMedCrossRefGoogle Scholar
  101. Prucca, C. G., Slavin, I., Quiroga, R., Elias, E. V., Rivero, F. D., Saura, A., Carranza, P. G., & Lujan, H. D. (2008). Antigenic variation in Giardia lamblia is regulated by RNA interference. Nature, 456, 750–754.PubMedCrossRefGoogle Scholar
  102. Ramesh, M. A., Malik, S. B., & Logsdon Jr., J. M. (2005). A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis. Current Biology, 15, 185–191.PubMedGoogle Scholar
  103. Reiner, D. S., McCaffery, M., & Gillin, F. D. (1990). Sorting of cyst wall proteins to a regulated secretory pathway during differentiation of the primitive eukaryote, Giardia lamblia. European Journal of Cell Biology, 53, 142–153.PubMedGoogle Scholar
  104. Rivero, M. R., Miras, S. L., Feliziani, C., Zamponi, N., Quiroga, R., Hayes, S. F., Ropolo, A. S., & Touz, M. C. (2012). Vacuolar protein sorting receptor in Giardia lamblia. PLoS One, 7, e43712.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Roger, A. J., Svard, S. G., Tovar, J., Clark, C. G., Smith, M. W., Gillin, F. D., & Sogin, M. L. (1998). A mitochondrial-like chaperonin 60 gene in Giardia lamblia: Evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proceedings of the National Academy of Sciences of the United States of America, 95, 229–234.PubMedPubMedCentralCrossRefGoogle Scholar
  106. Roxstrom-Lindquist, K., Jerlstrom-Hultqvist, J., Jorgensen, A., Troell, K., Svard, S. G., & Andersson, J. O. (2010). Large genomic differences between the morphologically indistinguishable diplomonads Spironucleus barkhanus and Spironucleus salmonicida. BMC Genomics, 11, 258.PubMedPubMedCentralCrossRefGoogle Scholar
  107. Sagolla, M. S., Dawson, S. C., Mancuso, J. J., & Cande, W. Z. (2006). Three-dimensional analysis of mitosis and cytokinesis in the binucleate parasite Giardia intestinalis. Journal of Cell Science, 119, 4889–4900.PubMedCrossRefGoogle Scholar
  108. Sangmaneedet, S., & Smith, S. A. (2000). In vitro studies on optimal requirements for the growth of Spironucleus vortens, an intestinal parasite of the freshwater angelfish. DisAquatOrgan, 39, 135–141.Google Scholar
  109. Scheltema, R. S. (1962). The relationship between the flagellate protozoon Hexamita and the oyster Crassostrea virginica. The Journal of Parasitology, 48, 137–141.PubMedCrossRefGoogle Scholar
  110. Schofield, P. J., Costello, M., Edwards, M. R., & O’Sullivan, W. J. (1990). The arginine dihydrolase pathway is present in Giardia intestinalis. International Journal for Parasitology, 20, 697–699.PubMedCrossRefGoogle Scholar
  111. Schupp, D. G., Januschka, M. M., Sherlock, L. A., Stibbs, H. H., Meyer, E. A., Bemrick, W. J., & Erlandsen, S. L. (1988). Production of viable Giardia cysts in vitro: Determination by fluorogenic dye staining, excystation, and animal infectivity in the mouse and Mongolian gerbil. Gastroenterology, 95, 1–10.PubMedCrossRefGoogle Scholar
  112. Shiflett, A. M., & Johnson, P. J. (2010). Mitochondrion-related organelles in eukaryotic protists. Annual Review of Microbiology, 64, 409–429.PubMedPubMedCentralCrossRefGoogle Scholar
  113. Simpson, A. G. (2003). Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). International Journal of Systematic and Evolutionary Microbiology, 53, 1759–1777.PubMedCrossRefGoogle Scholar
  114. Singer, S. M., & Nash, T. E. (2000). T-cell-dependent control of acute Giardia lamblia infections in mice. Infection and Immunity, 68, 170–175.PubMedPubMedCentralCrossRefGoogle Scholar
  115. Smith, P. D., Gillin, F. D., Spira, W. M., & Nash, T. E. (1982). Chronic giardiasis: Studies on drug sensitivity, toxin production, and host immune response. Gastroenterology, 83, 797–803.PubMedGoogle Scholar
  116. Sogin, M. L., Gunderson, J. H., Elwood, H. J., Alonso, R. A., & Peattie, D. A. (1989). Phylogenetic meaning of the kingdom concept: An unusual ribosomal RNA from Giardia lamblia. Science, 243, 75–77.PubMedCrossRefGoogle Scholar
  117. Spriegel, J. R., Saag, K. G., & Tsang, T. K. (1989). Infectious diarrhea secondary to Enteromonas hominis. The American Journal of Gastroenterology, 84, 1313–1314.PubMedGoogle Scholar
  118. Sterud, E. (1998). In vitro cultivation and temperature-dependent growth of two strains of Spironucleus barkhanus (Diplomonadida: Hexamitidae) from Atlantic salmon Salmo salar and grayling Thymallus thymallus. Diseases of Aquatic Organisms, 33, 57–61.PubMedCrossRefGoogle Scholar
  119. Svard, S. G., Meng, T. C., Hetsko, M. L., McCaffery, J. M., & Gillin, F. D. (1998). Differentiation-associated surface antigen variation in the ancient eukaryote Giardia lamblia. Molecular Microbiology, 30, 979–989.PubMedCrossRefGoogle Scholar
  120. Touz, M. C., Rivero, M. R., Miras, S. L., & Bonifacino, J. S. (2012). Lysosomal protein trafficking in Giardia lamblia: Common and distinct features. Frontiers in Bioscience, 4, 1898–1909.CrossRefGoogle Scholar
  121. Tovar, J., Leon-Avila, G., Sanchez, L. B., Sutak, R., Tachezy, J., van der Giezen, M., Hernandez, M., Muller, M., & Lucocq, J. M. (2003). Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature, 426, 172–176.PubMedCrossRefGoogle Scholar
  122. Tumova, P., Hofstetrova, K., Nohynkova, E., Hovorka, O., & Kral, J. (2007). Cytogenetic evidence for diversity of two nuclei within a single diplomonad cell of Giardia. Chromosoma, 116, 65–78.PubMedCrossRefGoogle Scholar
  123. Wiesehahn, G. P., Jarroll, E. L., Lindmark, D. G., Meyer, E. A., & Hallick, L. M. (1984). Giardia lamblia: Autoradiographic analysis of nuclear replication. Experimental Parasitology, 58, 94–100.PubMedCrossRefGoogle Scholar
  124. Williams, C. F., Millet, C. O., Hayes, A. J., Cable, J., & Lloyd, D. (2013). Diversity in mitochondrion-derived organelles of the parasitic diplomonads Spironucleus and Giardia. Trends in Parasitology, 29, 311–312.PubMedCrossRefGoogle Scholar
  125. Wood, A. M., & Smith, H. V. (2005). Spironucleosis (hexamitiasis, Hexamitosis) in the ring-necked pheasant (Phasianus colchicus): Detection of cysts and description of Spironucleus meleagridis in stained smears. Avian Diseases, 49, 138–143.PubMedCrossRefGoogle Scholar
  126. Xu, F., Jerlstrom-Hultqvist, J., & Andersson, J. O. (2012). Genome-wide analyses of recombination suggest that Giardia intestinalis assemblages represent different species. Molecular Biology and Evolution, 29, 2895–2898.PubMedCrossRefGoogle Scholar
  127. Xu, F., Jerlstrom-Hultqvist, J., Einarsson, E., Astvaldsson, A., Svard, S. G., & Andersson, J. O. (2014). The genome of Spironucleus salmonicida highlights a fish pathogen adapted to fluctuating environments. PLoS Genetics, 10, e1004053.PubMedPubMedCentralCrossRefGoogle Scholar
  128. Xu, F., Jerlstrom-Hultqvist, J., Kolisko, M., Simpson, A. G., Roger, A. J., Svard, S. G., & Andersson, J. O. (2016). On the reversibility of parasitism: Adaptation to a free-living lifestyle via gene acquisitions in the diplomonad Trepomonas sp. PC1. [Erratum appears in BMC Biol. 2016;14:77; PMID: 27619515] BMC Biology, 14, 62.PubMedPubMedCentralCrossRefGoogle Scholar
  129. Yang, Y., & Adam, R. D. (1994). Allele-specific expression of a variant-specific surface protein (VSP) of Giardia lamblia. Nucleic Acids Research, 22, 2102–2108.PubMedPubMedCentralCrossRefGoogle Scholar
  130. Yang, Y. M., & Adam, R. D. (1995). Analysis of a repeat-containing family of Giardia lamblia variant-specific surface protein genes: Diversity through gene duplication and divergence. The Journal of Eukaryotic Microbiology, 42, 439–444.PubMedCrossRefGoogle Scholar
  131. Yang, Y. M., Ortega, Y., Sterling, C., & Adam, R. D. (1994). Giardia lamblia Trophozoites contain multiple alleles of a variant-specific surface protein gene with 105-base pair tandem repeats. Molecular and Biochemical Parasitology, 68, 267–276.PubMedCrossRefGoogle Scholar
  132. Yu, L. Z., Birky Jr., C. W., & Adam, R. D. (2002). The two nuclei of Giardia each have complete copies of the genome and are partitioned equationally at cytokinesis. Eukaryotic Cell, 1, 191–199.PubMedPubMedCentralCrossRefGoogle Scholar
  133. Yubuki, N., Huang, S. S. C., & Leander, B. S. (2016). Comparative ultrastructure of fornicate excavates, including a novel free-living relative of diplomonads: Aduncisulcus paluster gen. et sp. nov. Protist, 167, 584–596.PubMedCrossRefGoogle Scholar
  134. Zwart, P., & Truyens, E. H. A. (1975). Hexamitiasis in tortoises. Veterinary Parasitology, 1, 175–183.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Aga Khan UniversityNairobiKenya
  2. 2.Professor EmeritusUniversity of Arizona, College of MedicineTucsonUSA

Personalised recommendations