Current Genetics

, Volume 51, Issue 3, pp 171–186

InterB multigenic family, a gene repertoire associated with subterminal chromosome regions of Encephalitozoon cuniculi and conserved in several human-infecting microsporidian species

  • Ndongo Dia
  • Laurence Lavie
  • Guy Méténier
  • Bhen S. Toguebaye
  • Christian P. Vivarès
  • Emmanuel Cornillot
Research Article

Abstract

Microsporidia are fungi-related obligate intracellular parasites that infect numerous animals, including man. Encephalitozoon cuniculi harbours a very small genome (2.9 Mbp) with about 2,000 coding sequences (CDSs). Most repeated CDSs are of unknown function and are distributed in subterminal regions that mark the transitions between subtelomeric rDNA units and chromosome cores. A potential multigenic family (interB) encoding proteins within a size range of 579–641 aa was investigated by PCR and RT-PCR. Thirty members were finally assigned to the E. cuniculi interB family and a predominant interB transcript was found to originate from a newly identified gene on chromosome III. Microsporidian species from eight different genera infecting insects, fishes or mammals, were tested for a possible intra-phylum conservation of interB genes. Only representatives of the Encephalitozoon, Vittaforma and Brachiola genera, differing in host range but all able to invade humans, were positive. Molecular karyotyping of Brachiola algerae showed a complex set of chromosome bands, providing a haploid genome size estimate of 15–20 Mbp. In spite of this large difference in genome complexity, B. algerae and E. cuniculi shared some similar interB gene copies and a common location of interB genes in near-rDNA subterminal regions.

Keywords

Encephalitozoon cuniculi Brachiola algerae Chromosome extremity Multigenic family KARD 2D-PFGE 

References

  1. Barry JD, Ginger ML, Burton P, McCulloch R (2003) Why are parasite contingency genes often associated with telomeres? Int J Parasitol 33:29–45PubMedCrossRefGoogle Scholar
  2. Baruch DI, Pasloske BL, Singh HB, Bi X, Ma XC, Feldman M, Taraschi TF, Howard RJ (1995) Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82:77–87PubMedCrossRefGoogle Scholar
  3. Beauvais B, Sarfati C, Challier S, Dérouin F (1994) In vitro model to assess effect of antimicrobial agents on Encephalitozoon cuniculi. Antimicrob Agents Chemother 38:2440–2448PubMedGoogle Scholar
  4. Becker M, Aitcheson N, Byles E, Wickstead B, Louis E, Rudenko G (2004) Isolation of the repertoire of VSG expression site containing telomeres of Trypanosoma brucei 427 using transformation-associated recombination in yeast. Genome Res 14:2319–2329PubMedCrossRefGoogle Scholar
  5. Biderre C, Pages M, Méténier G, David D, Bata J, Prensier G, Vivarès CP (1994) On small genomes in eukaryotic organisms: molecular karyotypes of two microsporidian species (Protozoa) parasites of vertebrates. C R Acad Sci III 317:399–404PubMedGoogle Scholar
  6. Biderre C, Canning E, Méténier G, Vivarès CP (1999a) Comparison of two isolates of Encephalitozoon hellem and E. intestinalis (Microspora) by pulsed field gel electrophoresis. Eur J Protistol 35:194–196Google Scholar
  7. Biderre C, Mathis A, Deplazes P, Weber R, Méténier G, Vivarès CP (1999b) Molecular karyotype diversity in the microsporidian Encephalitozoon cuniculi. Parasitology 118:439–445CrossRefGoogle Scholar
  8. Bohne W, Ferguson DJ, Kohler K, Gross U (2000) Developmental expression of a tandemly repeated, glycine- and serine-rich spore wall protein in the microsporidian pathogen Encephalitozoon cuniculi. Infect Immun 68:2268–2275PubMedCrossRefGoogle Scholar
  9. Brugère JF, Cornillot E, Méténier G, Bensimon A, Vivarès CP (2000a) Encephalitozoon cuniculi (Microspora) genome: physical map and evidence for telomere-associated rDNA units on all chromosomes. Nucleic Acids Res 28:2026–2033CrossRefGoogle Scholar
  10. Brugère JF, Cornillot E, Méténier G, Vivarès CP (2000b) In-gel DNA radiolabelling and two-dimensional pulsed field gel electrophoresis procedures suitable for fingerprinting and mapping small eukaryotic genomes. Nucleic Acids Res 28:E48CrossRefGoogle Scholar
  11. Brugère JF, Cornillot E, Méténier G, Vivarès CP (2000c) Occurrence of subtelomeric rearrangements in the genome of the microsporidian parasite Encephalitozoon cuniculi, as revealed by a new fingerprinting procedure based on two-dimensional pulsed field gel electrophoresis. Electrophoresis 21:2576–2581CrossRefGoogle Scholar
  12. Brugère JF, Cornillot E, Bourbon T, Méténier G, Vivarès CP (2001) Inter-strain variability of insertion/deletion events in the Encephalitozoon cuniculi genome: a comparative KARD-PFGE analysis. J Eukaryot Microbiol Suppl:50S–55SGoogle Scholar
  13. Cali A, Weiss LM, Takvorian PM (2004) An analysis of the microsporidian genus Brachiola, with comparisons of human and insect isolates of Brachiola algerae. J Eukaryot Microbiol 51:678–685PubMedCrossRefGoogle Scholar
  14. Castano I, Pan SJ, Zupancic M, Hennequin C, Dujon B, Cormack BP (2005) Telomere length control and transcriptional regulation of subtelomeric adhesins in Candida glabrata. Mol Microbiol 55:1246–1258PubMedCrossRefGoogle Scholar
  15. Corcoran LM, Thompson JK, Walliker D, Kemp DJ (1988) Homologous recombination within subtelomeric repeat sequences generates chromosome size polymorphisms in P. falciparum. Cell 53:807–813PubMedCrossRefGoogle Scholar
  16. Cornillot E, Keller B, Cushion MT, Méténier G, Vivarès CP (2002) Fine analysis of the Pneumocystis carinii f. sp. carinii genome by two-dimensional pulsed-field gel electrophoresis. Gene 293:87–95PubMedCrossRefGoogle Scholar
  17. Coyle CM, Weiss LM, Rhodes LV 3rd, Cali A, Takvorian PM, Brown DF, Visvesvara GS, Xiao L, Naktin J, Young E, Gareca M, Colasante G, Wittner M (2004) Fatal myositis due to the microsporidian Brachiola algerae, a mosquito pathogen. N Engl J Med 351:42–47PubMedCrossRefGoogle Scholar
  18. Croppo GP, Visvesvara GS, Leitch GJ, Wallace S, De Groote MA (1997) Western blot and immunofluorescence analysis of a human isolate of Encephalitozoon cuniculi established in culture from the urine of a patient with AIDS. J Parasitol 83:66–69PubMedCrossRefGoogle Scholar
  19. del Aguila C, Croppo GP, Moura H, Da Silva AJ, Leitch GJ, Moss DM, Wallace S, Slemenda SB, Pieniazek NJ, Visvesvara GS (1998) Ultrastructure, immunofluorescence, western blot and PCR analysis of eight isolates of Encephalitozoon (Septata) intestinalis established in culture from sputum and urine samples and duodenal aspirates of five patients with AIDS. J Clin Microbiol 36:1201–1208Google Scholar
  20. Delbac F, Peyret P, Méténier G, David D, Danchin A, Vivarès CP (1998) On proteins of the microsporidian invasive apparatus: complete sequence of a polar tube protein of Encephalitozoon cuniculi. Mol Microbiol 29:825–834PubMedCrossRefGoogle Scholar
  21. Delbac F, Peuvel I, Méténier G, Peyretaillade E, Vivarès CP (2001) Microsporidian invasion apparatus: identification of a novel polar tube protein and evidence for clustering of ptp1 and ptp2 genes in three Encephalitozoon species. Infect Immun 69:1016–1024PubMedCrossRefGoogle Scholar
  22. Desportes I, Le Charpentier Y, Galian A, Bernard F, Cochand-Priollet B, Lavergne A, Ravisse P, Modigliani R (1985) Occurrence of a new microsporidan: Enterocytozoon bieneusi n.g., n. sp., in the enterocytes of a human patient with AIDS. J Protozool 32:250–254PubMedGoogle Scholar
  23. Didier ES, Stovall ME, Green LC, Brindley PJ, Sestak K, Didier PJ (2004) Epidemiology of microsporidiosis: sources and modes of transmission. Vet Parasitol 126:145–166PubMedCrossRefGoogle Scholar
  24. Faye N, Toguebaye BS, Bouix G (1994) Nosemoides syacii n.sp., a microsporidian parasite of the West African turbot Syacium micrurum Ranzani, 1840. Syst parasitol 29:43–50Google Scholar
  25. Freitas-Junior LH, Hernandez-Rivas R, Ralph SA, Montiel-Condado D, Ruvalcaba-Salazar OK, Rojas-Meza AP, Mancio-Silva L, Leal-Silvestre RJ, Montijo AM, Shorte S, Scherf A (2005) Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 121:25–36PubMedCrossRefGoogle Scholar
  26. Halme A, Bumgarner S, Styles C, Fink GR (2004) Genetic and epigenetic regulation of the FLO gene family generates cell-surface variation in yeast. Cell 116:405–415PubMedCrossRefGoogle Scholar
  27. Jouvenaz DP (1981) Percoll: an effective medium for cleaning microsporidian spores. J Invertebr Pathol 37:319CrossRefGoogle Scholar
  28. Katinka MD, Duprat S, Cornillot E, Méténier G, Thomarat F, Prensier G, Barbe V, Peyretaillade E, Brottier P, Wincker P, Delbac F, El Alaoui H, Peyret P, Saurin W, Gouy M, Weissenbach J, Vivarès CP (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450–453PubMedCrossRefGoogle Scholar
  29. Kawakami Y, Inoue T, Ito K, Kitamizu K, Hanawa C, Ando T, Iwano H, Ishihara R (1994) Identification of a chromosome harbouring the small subunit ribosomal RNA gene of Nosema bombycis. J Invertebr Pathol 64:147–148PubMedCrossRefGoogle Scholar
  30. Kucerova Z, Moura H, Visvesvara GS, Leitch GJ (2004) Differences between Brachiola (Nosema) algerae isolates of human and insect origin when tested using an in vitro spore germination assay and a cultured cell infection assay. J Eukaryot Microbiol 51:339–343PubMedCrossRefGoogle Scholar
  31. Lalor TM, Kjeldgaard M, Shimamoto GT, Strickler JE, Konigsberg WH, Richards FF (1984) Trypanosome variant-specific glycoproteins: a polygene protein family with multiple folding patterns? Proc Natl Acad Sci USA 81:998–1002PubMedCrossRefGoogle Scholar
  32. Lowman PM, Takvorian PM, Cali A (2000) The effects of elevated temperatures and various time-temperature combinations on the development of Brachiola (Nosema) algerae N. Comb. in mammalian cell culture. J Eukaryot Microbiol 47:221–234PubMedCrossRefGoogle Scholar
  33. Mansour L, Cheikali C, Desaunais P, Coulon JP, Daubin J, Hassine OK, Vivares CP, Jeanjean J, Cornillot E (2004) Description of an ultrathin multiwire proportional chamber-based detector and application to the characterization of the Spraguea lophii (Microspora) two-dimensional genome fingerprint. Electrophoresis 25:3365–77PubMedCrossRefGoogle Scholar
  34. Mathis A, Michel M, Kuster H, Muller C, Weber R, Deplazes P (1997) Two Encephalitozoon cuniculi strains of human origin are infectious to rabbits. Parasitology 114:29–35PubMedCrossRefGoogle Scholar
  35. Mathis A, Weber R, Deplazes P (2005) Zoonotic potential of the microsporidia. Clin Microbiol Rev 18:423–445PubMedCrossRefGoogle Scholar
  36. Melville SE, Leech V, Gerrard CS, Tait A, Blackwell JM (1998) The molecular karyotype of the megabase chromosomes of Trypanosoma brucei and the assignment of chromosome markers. Mol Biochem Parasitol 94:155–173PubMedCrossRefGoogle Scholar
  37. Moretto M, Weiss LM, Khan IA (2004) Induction of a rapid and strong antigen-specific intraepithelial lymphocyte response during oral Encephalitozoon cuniculi infection. J Immunol 172:4402–4409PubMedGoogle Scholar
  38. Müller A, Trammer T, Chioralia G, Seitz HM, Diehl V, Franzen C (2000) Ribosomal RNA of Nosema algerae and phylogenetic relationship to other microsporidia. Parasitol Res 86:18–23PubMedCrossRefGoogle Scholar
  39. Nassonova E, Cornillot E, Méténier G, Agafonova N, Kudryavtsev B, Skarlato S, Vivarès CP (2005) Chromosomal composition of the genome in the monomorphic diplokaryotic microsporidium Paranosema grylli: analysis by two-dimensional pulsed-field gel electrophoresis. Folia Parasitol (Praha) 52:145–57Google Scholar
  40. Pays E (2005) Regulation of antigen gene expression in Trypanosoma brucei. Trends Parasitol 21:517–520PubMedCrossRefGoogle Scholar
  41. Peuvel I, Delbac F, Méténier G, Peyret P, Vivarès CP (2000) Polymorphism of the gene encoding a major polar tube protein PTP1 in two microsporidia of the genus Encephalitozoon. Parasitology 121:581–587PubMedCrossRefGoogle Scholar
  42. Peuvel I, Peyret P, Méténier G, Vivarès CP, Delbac F (2002) The microsporidian polar tube: evidence for a third polar tube protein (PTP3) in Encephalitozoon cuniculi. Mol Biochem Parasitol 122:69–80PubMedCrossRefGoogle Scholar
  43. Peuvel-Fanget I, Polonais V, Brosson D, Texier C, Kuhn L, Peyret P, Vivarès C, Delbac F (2006) EnP1 and EnP2, two proteins associated with the Encephalitozoon cuniculi endospore, the chitin-rich inner layer of the microsporidian spore wall. Int J Parasitol 36:309–318PubMedCrossRefGoogle Scholar
  44. Pryde FE, Gorham HC, Louis EJ (1997) Chromosome ends: all the same under their caps. Curr Opin Genet Dev 7:822–828PubMedCrossRefGoogle Scholar
  45. Ralph SA, Scherf A (2005) The epigenetic control of antigenic variation in Plasmodium falciparum. Curr Opin Microbiol 8:434–440PubMedCrossRefGoogle Scholar
  46. Sato R, Watanabe H (1980) Purification of mature microsporidian spores by isodensity equilibrium centrifugate. Journal of Sericulture Science Jpn 49:512–516Google Scholar
  47. Schwartz DA, Visvesvara GS, Diesenhouse MC, Weber R, Font RL, Wilson LA, Corrent G, Serdarevic ON, Rosberger DF, Keenen PC, Grossniklaus HE, Hewan-Lowe K, Bryan RT (1993) Pathologic features and immunofluorescent antibody demonstration of ocular microsporidiosis (Encephalitozoon hellem) in seven patients with acquired immunodeficiency syndrome. Am J Ophthalmol 115:285–292PubMedGoogle Scholar
  48. Slamovits CH, Williams BA, Keeling PJ (2004) Transfer of Nosema locustae (Microsporidia) to Antonospora locustae n. comb. based on molecular and ultrastructural data. J Eukaryot Microbiol 51:207–213PubMedCrossRefGoogle Scholar
  49. Sokolova YY, Dolgikh VV, Morzhina EV, Nassonova ES, Issi IV, Terry RS, Ironside JE, Smith JE, Vossbrinck CR (2003) Establishment of the new genus Paranosema based on the ultrastructure and molecular phylogeny of the type species Paranosema grylli Gen. Nov., Comb. Nov. (Sokolova, Selezniov, Dolgikh, Issi 1994), from the cricket Gryllus bimaculatus Deg. J Invertebr Pathol 84:159–172PubMedCrossRefGoogle Scholar
  50. Stechmann A (2004) Genome evolution: the dynamics of static genomes. Curr Biol 14:473–474CrossRefGoogle Scholar
  51. Vavra J, Undeen AH (1970) Nosema algerae n. sp. (Cnidospora, Microsporida) a pathogen in a laboratory colony of Anopheles stephensi Liston (Diptera, Culicidae). J Protozool 17:240–249PubMedGoogle Scholar
  52. Visvesvara GS, Moura H, Leitch GJ, Schwartz DA, Xiao LX (2005) Public health importance of Brachiola algerae (Microsporidia)–an emerging pathogen of humans. Folia Parasitol (Praha) 52:83–94Google Scholar
  53. Vossbrinck CR, Debrunner-Vossbrinck BA (2005) Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitol (Praha) 52:131–142Google Scholar
  54. Weidner E, Canning EU, Rutledge CR, Meek CL (1999) Mosquito (Diptera: Culicidae) host compatibility and vector competency for the human myositic parasite Trachipleistophora hominis (Phylum Microspora). J Med Entomol 36:522–525PubMedGoogle Scholar
  55. Xiao L, Li L, Moura H, Sulaiman I, Lal AA, Gatti S, Scaglia M, Didier ES, Visvesvara GS (2001) Genotyping Encephalitozoon hellem isolates by analysis of the polar tube protein gene. J Clin Microbiol 39:2191–2196PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Ndongo Dia
    • 1
  • Laurence Lavie
    • 1
  • Guy Méténier
    • 1
  • Bhen S. Toguebaye
    • 2
  • Christian P. Vivarès
    • 1
  • Emmanuel Cornillot
    • 1
  1. 1.Equipe Parasitologie Moléculaire et Cellulaire, Laboratoire de Biologie des ProtistesUMR CNRS 6023, Bâtiment Biologie A, Université Blaise PascalAubière cedexFrance
  2. 2.Laboratoire de Parasitologie Générale, Département de Biologie Animale, Faculté des Sciences et TechnologiesUniversité Cheikh Anta DiopDakarSenegal

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