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

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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.

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References

  • Barry JD, Ginger ML, Burton P, McCulloch R (2003) Why are parasite contingency genes often associated with telomeres? Int J Parasitol 33:29–45

    Article  PubMed  CAS  Google Scholar 

  • 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 82:77–87

    Article  PubMed  CAS  Google Scholar 

  • Beauvais B, Sarfati C, Challier S, Dérouin F (1994) In vitro model to assess effect of antimicrobial agents on Encephalitozoon cuniculi. Antimicrob Agents Chemother 38:2440–2448

    PubMed  CAS  Google Scholar 

  • 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 14:2319–2329

    Article  PubMed  CAS  Google Scholar 

  • 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 317:399–404

    PubMed  CAS  Google Scholar 

  • 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 35:194–196

    Google Scholar 

  • Biderre C, Mathis A, Deplazes P, Weber R, Méténier G, Vivarès CP (1999b) Molecular karyotype diversity in the microsporidian Encephalitozoon cuniculi. Parasitology 118:439–445

    Article  CAS  Google Scholar 

  • 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 68:2268–2275

    Article  PubMed  CAS  Google Scholar 

  • 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 28:2026–2033

    Article  Google Scholar 

  • 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:E48

    Article  Google Scholar 

  • 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 21:2576–2581

    Article  Google Scholar 

  • 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–55S

  • 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 51:678–685

    Article  PubMed  Google Scholar 

  • 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 55:1246–1258

    Article  PubMed  CAS  Google Scholar 

  • Corcoran LM, Thompson JK, Walliker D, Kemp DJ (1988) Homologous recombination within subtelomeric repeat sequences generates chromosome size polymorphisms in P. falciparum. Cell 53:807–813

    Article  PubMed  CAS  Google Scholar 

  • 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 293:87–95

    Article  PubMed  CAS  Google Scholar 

  • 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 351:42–47

    Article  PubMed  CAS  Google Scholar 

  • 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 83:66–69

    Article  PubMed  CAS  Google Scholar 

  • 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 36:1201–1208

    Google Scholar 

  • 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 29:825–834

    Article  PubMed  CAS  Google Scholar 

  • 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 69:1016–1024

    Article  PubMed  CAS  Google Scholar 

  • 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 32:250–254

    PubMed  CAS  Google Scholar 

  • Didier ES, Stovall ME, Green LC, Brindley PJ, Sestak K, Didier PJ (2004) Epidemiology of microsporidiosis: sources and modes of transmission. Vet Parasitol 126:145–166

    Article  PubMed  CAS  Google Scholar 

  • 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 29:43–50

    Google Scholar 

  • 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 121:25–36

    Article  PubMed  CAS  Google Scholar 

  • 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 116:405–415

    Article  PubMed  CAS  Google Scholar 

  • Jouvenaz DP (1981) Percoll: an effective medium for cleaning microsporidian spores. J Invertebr Pathol 37:319

    Article  Google Scholar 

  • 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 414:450–453

    Article  PubMed  CAS  Google Scholar 

  • 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 64:147–148

    Article  PubMed  CAS  Google Scholar 

  • 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 51:339–343

    Article  PubMed  Google Scholar 

  • 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 81:998–1002

    Article  PubMed  CAS  Google Scholar 

  • 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 47:221–234

    Article  PubMed  CAS  Google Scholar 

  • 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 25:3365–77

    Article  PubMed  CAS  Google Scholar 

  • 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 114:29–35

    Article  PubMed  Google Scholar 

  • Mathis A, Weber R, Deplazes P (2005) Zoonotic potential of the microsporidia. Clin Microbiol Rev 18:423–445

    Article  PubMed  CAS  Google Scholar 

  • 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 94:155–173

    Article  PubMed  CAS  Google Scholar 

  • 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 172:4402–4409

    PubMed  CAS  Google Scholar 

  • 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 86:18–23

    Article  PubMed  Google Scholar 

  • 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) 52:145–57

    CAS  Google Scholar 

  • Pays E (2005) Regulation of antigen gene expression in Trypanosoma brucei. Trends Parasitol 21:517–520

    Article  PubMed  CAS  Google Scholar 

  • 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 121:581–587

    Article  PubMed  CAS  Google Scholar 

  • 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 122:69–80

    Article  PubMed  CAS  Google Scholar 

  • 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 36:309–318

    Article  PubMed  CAS  Google Scholar 

  • Pryde FE, Gorham HC, Louis EJ (1997) Chromosome ends: all the same under their caps. Curr Opin Genet Dev 7:822–828

    Article  PubMed  CAS  Google Scholar 

  • Ralph SA, Scherf A (2005) The epigenetic control of antigenic variation in Plasmodium falciparum. Curr Opin Microbiol 8:434–440

    Article  PubMed  CAS  Google Scholar 

  • Sato R, Watanabe H (1980) Purification of mature microsporidian spores by isodensity equilibrium centrifugate. Journal of Sericulture Science Jpn 49:512–516

    Google Scholar 

  • 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 115:285–292

    PubMed  CAS  Google Scholar 

  • 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 51:207–213

    Article  PubMed  CAS  Google Scholar 

  • 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 84:159–172

    Article  PubMed  CAS  Google Scholar 

  • Stechmann A (2004) Genome evolution: the dynamics of static genomes. Curr Biol 14:473–474

    Article  Google Scholar 

  • 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 17:240–249

    PubMed  CAS  Google Scholar 

  • 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) 52:83–94

    Google Scholar 

  • Vossbrinck CR, Debrunner-Vossbrinck BA (2005) Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitol (Praha) 52:131–142

    CAS  Google Scholar 

  • 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 36:522–525

    PubMed  CAS  Google Scholar 

  • 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 39:2191–2196

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank all people who provided us with either DNA or spores from microsporidia that were not available in the Clermont-Fd laboratory: Drs Lamjed Mansour for Glugea atherinae and Spraguea lophii, Ngor Faye for Neonosemoïdes syacii, Elena Nassonova for Paranosema grylli and Wang Lin for Nosema bombycis. We convey our special thanks to Drs Elisabeth S. Didier and Lisa C. Bowers for sending Vittaforma corneae spores despite the fact that these persons were affected by Katrina hurricane. We also thank Dr. Damien Brosson for helpful discussion. This work was supported by grants from EGIDE France (Ndongo Dia PhD) and the Medical Research Foundation (FRM: Fondation pour la Recherche Médicale; Laurence Lavie post-doctoral position).

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Correspondence to Emmanuel Cornillot.

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Communicated by S. Michaeli.

The members of the genus Brachiola have been transferred to the genus Anncaliia [Franzen et al. (2006) J Eukaryot Microbiol 53:26–35].

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Dia, N., Lavie, L., Méténier, G. et al. InterB multigenic family, a gene repertoire associated with subterminal chromosome regions of Encephalitozoon cuniculi and conserved in several human-infecting microsporidian species. Curr Genet 51, 171–186 (2007). https://doi.org/10.1007/s00294-006-0114-x

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  • DOI: https://doi.org/10.1007/s00294-006-0114-x

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