Skip to main content
SpringerLink
Log in

Cytogenetic evidence for diversity of two nuclei within a single diplomonad cell of Giardia

  • Research Article
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Giardia intestinalis is an ancient protist that causes the most commonly reported human diarrheal disease of parasitic origin worldwide. An intriguing feature of the Giardia cell is the presence of two morphologically similar nuclei, generally considered equivalent, in spite of the fact that their karyotypes are unknown. We found that within a single cell, the two nuclei differ both in the number and the size of chromosomes and that representatives of two major genetic groups of G. intestinalis possess different karyotypes. Odd chromosome numbers indicate aneuploidy of Giardia nuclei, and their stable occurrence is suggestive of a long-term asexuality. A semi-open type of Giardia mitosis excludes a chromosome interfusion between the nuclei. Differences in karyotype and DNA content, and cell cycle-dependent asynchrony are indicative of diversity of the two Giardia nuclei.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Adam RD (1992) Chromosome-size variation in Giardia lamblia—the role of rDNA repeats. Nucleic Acids Res 20:3057–3061

    Article  PubMed  CAS  Google Scholar 

  • Adam RD (2000) The Giardia lamblia genome. Int J Parasitol 20:475–484

    Article  Google Scholar 

  • Adam RD (2001) Biology of Giardia lamblia. Clin Microbiol Rev 14:447–475

    Article  PubMed  CAS  Google Scholar 

  • Adam RD, Nash TE, Wellems TE (1988) The Giardia lamblia trophozoite contains sets of closely related chromosomes. Nucleic Acids Res 16:4555–4567

    Article  PubMed  CAS  Google Scholar 

  • Ali SA, Hill DR (2003) Giardia intestinalis. Curr Opin Infect Dis 16:453–460

    Article  PubMed  Google Scholar 

  • Arkhipova IR, Morrison HG (2001) Three retrotransposon families in the genome of Giardia lamblia: two telomeric, one dead. Proc Natl Acad Sci U S A 98:14497–14502

    Article  PubMed  CAS  Google Scholar 

  • Baruch AC, Isaac-Renton J, Adam RD (1996) The molecular epidemiology of Giardia lamblia: a sequence-based approach. J Infect Dis 174:233–236

    PubMed  CAS  Google Scholar 

  • Bernander R, Palm JED, Svärd SG (2001) Genome ploidy in different stages of the Giardia lamblia life cycle. Cell Microbiol 3:55–62

    Article  PubMed  CAS  Google Scholar 

  • Birky CW (2005) Sex: is Giardia doing it in the dark? Curr Biol 15:56–58

    Article  CAS  Google Scholar 

  • Brugerolle G (1975) Contribution à l´étude cytologique et phylétique des diplozoaires (Zoomastigophorea, Diplozoa, Dangeard 1910). V. Nouvelle interprétation de l´organisation cellulaire de Giardia. Protistologica 11:99–109

    Google Scholar 

  • Brugerolle G (1991) Flagellar and cytoskeletal systems in amitochondrial flagellates: Archamoeba, Metamonada and Parabasala. Protoplasma 164:70–90

    Article  Google Scholar 

  • Cavalier-Smith T (1995) Cell cycles, diplokaryosis and the archezoan origin of sex. Arch Protistenkd 145:189–207

    Google Scholar 

  • Červa L, Nohýnková E (1992) A light microscopic study of the course of cellular division of Giardia intestinalis trophozoites grown in vitro. Folia Parasitol 39:97–104

    PubMed  Google Scholar 

  • Coppel RL, Black CG (2005) Parasite genomes. Int J Parasitol 35:465–479

    Article  PubMed  CAS  Google Scholar 

  • Elmendorf HG, Singer SM, Nash TE (2000) Targeting of proteins to the nuclei of Giardia lamblia. Mol Biochem Parasitol 106:315–319

    Article  PubMed  CAS  Google Scholar 

  • Elmendorf HG, Dawson SC, McCaffery JM (2003) The cytoskeleton of Giardia lamblia. Int J Parasitol 33:3–28

    Article  PubMed  Google Scholar 

  • Erlandsen SL, Rasch EM (1994) The DNA content of trophozoites and cysts of Giardia lamblia by microdensitometric quantitation of Feulgen staining and examination by laser scanning confocal microscopy. J Histochem Cytochem 42:1413–1416

    PubMed  CAS  Google Scholar 

  • Ersfeld K, Melville SE, Gull K (1999) Nuclear and genome organization of Trypanosoma brucei. Parasitol Today 15:58–63

    Article  PubMed  CAS  Google Scholar 

  • Fan JB, Korman SH, Cantor CR, Smith CL (1991) Giardia lamblia: haploid genome size determined by pulse field gel electrophoresis is less than 12 Mb. Nucleic Acids Res 19:1905–1908

    Article  PubMed  CAS  Google Scholar 

  • Filice FP (1952) Studies on the cytology and life history of a Giardia from the laboratory rat. Univ Calif Publ Zool 57:53–146

    Google Scholar 

  • Gaunt MW, Yeo M, Frame IA, Stothard JR, Carrasco HJ, Taylor MC, Mena SS, Veazey P, Miles GAJ, Acosta N, Arias AR, Miles MA (2003) Mechanism of genetic exchange in American trypanosomes. Nature 421:936–939

    Article  PubMed  CAS  Google Scholar 

  • Gillin FD, Boucher SE, Rossi SS, Reiner DS (1989) Giardia lamblia: the roles of bile, lactic acid, and pH in the completion of the life cycle in vitro. Exp Parasitol 69:164-174

    Article  PubMed  CAS  Google Scholar 

  • Gillin DF, Reiner DS, McCaffery JM (1996) Cell biology of the primitive eukaryote Giardia lamblia. Annu Rev Microbiol 50:679–705

    Article  PubMed  CAS  Google Scholar 

  • Gong N, Yang H, Zhang G, Landau BJ, Guo X (2004) Chromosome inheritance in triploid Pacific oyster Crassostrea gigas Thunberg. Heredity 93:408–415

    Article  PubMed  CAS  Google Scholar 

  • Gottesfeld JM, Forbes DJ (1997) Mitotic repression of the transcriptional machinery. Trends Biochem Sci 22:197–202

    Article  PubMed  CAS  Google Scholar 

  • Gull K, Alsford S, Ersfeld K (1998) Segregation of minichromosomes in trypanosomes: implications for mitotic mechanisms. Trends Microbiol 6:319–323

    Article  PubMed  CAS  Google Scholar 

  • Hou G, Le Blancq M, Yaping E, Zhu H, Lee MG (1995) Structure of a frequently rearranged rRNA-encoding chromosome in Giardia lamblia. Nucleic Acids Res 23:3310–3317

    Article  PubMed  CAS  Google Scholar 

  • Kabnick KS, Peattie DA (1990) In situ analyses reveal that the two nuclei of Giardia lamblia are equivalent. J Cell Sci 95:353–360

    PubMed  Google Scholar 

  • Keister DB (1983) Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 77:487–488

    Article  PubMed  CAS  Google Scholar 

  • Kofoid CA, Christiansen EB (1915) On binary and multiple fission in Giardia muris (Grassi). Univ Calif Publ Zool 16:30–54

    Google Scholar 

  • 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. Int J Syst Evol Microbiol 55:1729–1733

    Article  PubMed  CAS  Google Scholar 

  • Le Blancq SM, Adam RD (1998) Structural basis for karyotype heterogeneity in Giardia lamblia. Mol Biochem Parasitol 97:199–208

    Article  PubMed  Google Scholar 

  • Lloyd D, Harris JC (2002) Giardia: highly evolved parasite or early branching eukaryote? Trends Microbiol 10:122–127

    Article  PubMed  CAS  Google Scholar 

  • McArthur AG, Morrison HG, Nixon JEJ, Passamaneck NQE, Kim U, Hinkle G, Crocker MK, Holder ME, Farr R, Reich CI et al (2000) The Giardia genome project database. FEMS Microbiol Lett 189:271–273

    Article  PubMed  CAS  Google Scholar 

  • Monis PT, Mayerhofer G, Andrews RH, Homan WL, Limper L, Ey PL (1996) Molecular genetic analysis of Giardia intestinalis isolates at the glutamate dehydrogenase locus. Parasitology 112:1–12

    Article  PubMed  CAS  Google Scholar 

  • Monis PT, Andrews RH, Mayerhofer G, Ey PL (2003) Genetic diversity within the morphological species Giardia intestinalis and its relationship to host origin. Infect Genet Evol 3:29–38

    Article  PubMed  CAS  Google Scholar 

  • Nohýnková E, Dráber P, Reischig J, Kulda J (2000) Localization of gamma-tubulin in interphase and mitotic cells of a unicellular eukaryote, Giardia intestinalis. Eur J Cell Biol 79:438–445

    Article  PubMed  Google Scholar 

  • Nohýnková E, Tůmová P, Kulda J (2006) Cell division of Giardia intestinalis: flagellar developmental cycle involves transformation and exchange of flagella between mastigonts of a diplomonad cell. Eukaryot Cell 5:753–761

    Article  PubMed  CAS  Google Scholar 

  • Passarge E (1974) Analysis of chromosomes in mitosis and evaluation of cytogenetic data. In: Schwarzacher HG, Wolf U (eds) Methods in human cytogenetics. Springer, Berlin Heidelberg New York, pp 135–205

    Google Scholar 

  • Prowazek S, Werner H (1914) Zur Kenntnis der sog. Flagellaten. Arch Schiffs Tropenhyg 18:311–326

    Google Scholar 

  • Raikov IB (1982) The protozoan nucleus. Morphology and evolution. Springer Verlag, Wien, New York

  • Raikov IB (1994) The diversity of forms of mitosis in Protozoa: a comparative review. Eur J Protistol 30:253–269

    Google Scholar 

  • Ramesh MA, Malik SB, Logsdon JM (2005) A phylogenetic inventory of meiotic genes: evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr Biol 15:185–191

    PubMed  CAS  Google Scholar 

  • Ravel C, Debussay P, Blackwell JM, Ivens AC, Bastien P (1998) The complete chromosomal organization of the reference strain of the Leishmania genome project, L.major ‘Friedlin’. Parasitol Today 14:301–303

    Article  PubMed  Google Scholar 

  • Rodenwaldt E (1912) Flagellaten (Trichomonas, Lamblia). In: von Prowazek S (ed) Handbuch der Pathogenen Protozoen. Barth, Leipzig

  • Roger AJ, Svärd SG, Tovar J, Clark CG, Smith MW, Gillin FD, Sogin ML (1998) A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc Natl Acad Sci U S A 95:229–234

    Article  PubMed  CAS  Google Scholar 

  • Rosenbusch B (2004) The incidence of aneuploidy in human oocytes assessed by conventional cytogenetic analysis. Hereditas 141:97–105

    Article  PubMed  Google Scholar 

  • Siddall ME, Hong H, Desser SS (1992) Phylogenetic analysis of the Diplomonadida (Wenyon, 1926) Brugerolle, 1975: evidence for heterochrony in protozoa and against Giardia lamblia as a “missing link”. J Protozool 39:361–367

    PubMed  CAS  Google Scholar 

  • Sola L, Rossi AR, Iaselli V, Rasch EM, Monaco PJ (1992) Cytogenetics of bisexual/unisexual species of Poecilia. II. Analysis of heterochromatin and nucleolar organizer regions in Poecilia mexicana mexicana by C-banding and DAPI, quinacrine, chromomycin A3, and silver staining. Cytogenet Cell Genet 60:229–235

    Article  PubMed  CAS  Google Scholar 

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306

    Article  PubMed  CAS  Google Scholar 

  • Svärd SG, Hagblom P, Palm JED (2003) Giardia lamblia—a model organism for eukaryotic cell differentiation. FEMS Microbiol Lett 218:3–7

    Article  PubMed  Google Scholar 

  • Šedinová J, Flegr J, Ey P, Kulda J (2003) Use of random amplified polymorphic DNA (RAPD) analysis for the identification of Giardia intestinalis subtypes and phylogenetic tree construction. J Eukaryot Microbiol 50:198–203

    Article  PubMed  Google Scholar 

  • Taylor SS, Scott MIF, Holland AJ (2004) The spindle checkpoint: a quality control mechanism which ensures accurate chromosome segregation. Chromosome Res 12:599–616

    Article  PubMed  CAS  Google Scholar 

  • Thompson RCA, Monis PT (2004) Variation in Giardia: implications for taxonomy and epidemiology. Adv Parasitol 58:69–137

    PubMed  CAS  Google Scholar 

  • Tibayrenc M, Ayala FJ (2002) The clonal theory of parasitic protozoa: 12 years on. Trends Parasitol 18:405–410

    Article  PubMed  CAS  Google Scholar 

  • Tovar J, Leon-Avila G, Sanchez LB, Šuták R, Tachezy J, Giezen N, Hernandez M, Miller M, Lucocq JM (2003) Mitochondrial remnant organelles of Giardia intestinalis function in iron sulphur protein maturation. Nature 426:172–174

    Article  PubMed  CAS  Google Scholar 

  • Upcroft JA, Chen NH, Upcroft P (1996) Mapping variation in chromosome homologues of different Giardia strains. Mol Biochem Parasitol 76:135–143

    Article  PubMed  CAS  Google Scholar 

  • Upcroft P, Upcroft JA (1994) Two distinct varieties of Giardia in a mixed infection from a single human patient. J Eukaryot Microbiol 41:189–194

    Article  PubMed  CAS  Google Scholar 

  • Upcroft P, Upcroft JA (1999) Organization and structure of the Giardia genome. Protist 150:17–23

    Article  PubMed  CAS  Google Scholar 

  • Upcroft JA, Abedinia M, Upcroft P (2005) Rearranged subtelomeric rRNA genes in Giardia duodenalis. Eukaryot Cell 4:484–486

    Article  PubMed  CAS  Google Scholar 

  • Wickstead B, Ersfeld K, Gull K (2003) Repetitive elements in genomes of parasitic protozoa. Microbiol Mol Biol Rev 67:360–375

    Article  PubMed  CAS  Google Scholar 

  • Wiesehahn GP, Jarroll EL, Lindmark DG, Meyer EA, Hallick LM (1984) Giardia lamblia: autoradiographic analysis of nuclear replication. Exp Parasitol 58:94–100

    Article  PubMed  CAS  Google Scholar 

  • Yang YM, Adam RD (1994) Allele-specific expression of a variant-specific surface protein (VSP) of Giardia lamblia. Nucleic Acids Res 22:2102–2108

    Article  PubMed  CAS  Google Scholar 

  • Yang YM, Adam RD (1995) A group of Giardia lamblia variant-specific surface protein (VSP) genes with nearly identical 5′ regions. Mol Biochem Parasitol 75:69–74

    Article  PubMed  CAS  Google Scholar 

  • Yu LZ, Birky CW, Adam RD (2002) The two nuclei of Giardia each have complete copies of the genome and are partitioned equationally at cytokinesis. Eukaryot Cell 1:191–199

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

We thank Jaroslav Flegr, Petr Lonský, Roman Krejčí, František Št’áhlavský (Charles University, Prague), and Shin Jyh-Wei (National Cheng Kung University, Taiwan) for their assistance in evaluating karyological data, and we also thank Masataka Kawai (University of Iowa, IA, USA) for reading the manuscript. The study was supported by Research Projects 0021620806 (P.T., E.N.) and 0021620828 (J.K.) from the Ministry of Education of the Czech Republic and 310/05/H533 (K.H.) from the Grant Agency of the Czech Republic.

Author information

Authors and Affiliations

  1. Department of Tropical Medicine, First Faculty of Medicine, Charles University in Prague, Studničkova 7, Prague 2, 12800, Czech Republic

    Pavla Tůmová, Klára Hofštetrová & Eva Nohýnková

  2. Institute of Microbiology, Academy of Sciences, Prague, Czech Republic

    Ondřej Hovorka

  3. Department of Genetics and Microbiology, Charles University in Prague, Prague, Czech Republic

    Jiří Král

Authors
  1. Pavla Tůmová
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Klára Hofštetrová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eva Nohýnková
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ondřej Hovorka
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jiří Král
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pavla Tůmová.

Additional information

Communicated by E.A. Nigg

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tůmová, P., Hofštetrová, K., Nohýnková, E. et al. Cytogenetic evidence for diversity of two nuclei within a single diplomonad cell of Giardia . Chromosoma 116, 65–78 (2007). https://doi.org/10.1007/s00412-006-0082-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-006-0082-4

Keywords

Search

Navigation