Phylogenetic approach to the variability of the microsporidian enterocytozoon bieneusi and its implications for inter- and intrahost transmission

Applied and Environmental Microbiology

Volumn 76, Issue 10, 2010, Pages 3333-3342

  Henriques Gil, Nuno ^a   Haro, María ^a   Izquierdo, Fernando ^a   Fenoy, Soledad ^a   Águilat, Carmen Del ^a  

^a UNIVERSIDAD SAN PABLO CEU   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

FOUR-GROUP; GEOGRAPHICAL ORIGINS; HAPLOTYPES; HOST-SPECIFICITY; HUMAN INFECTION; INTERNAL TRANSCRIBED SPACERS; PARASITE-; PHYLOGENETIC APPROACH; PHYLOGENETIC STUDIES; STRAIN EVOLUTION; WILD ANIMALS;

ANIMALS;

RIBOSOMAL SPACER DNA;

ALLELE; EUKARYOTE; GENETIC ANALYSIS; GENOTYPE; HOST SPECIFICITY; INFECTIVITY; PARASITE; PARASITE INFESTATION; PHYLOGENETICS; PHYLOGEOGRAPHY;

ANIMAL; ARTICLE; CATTLE; CATTLE DISEASE; CLASSIFICATION; DISEASE TRANSMISSION; ENTEROCYTOZOON; GENETIC VARIABILITY; GENETICS; GENOTYPE; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROSPORIDIOSIS; PHYLOGENY; SWINE; SWINE DISEASE; WILD ANIMAL;

ANIMALS; ANIMALS, WILD; CATTLE; CATTLE DISEASES; DNA, RIBOSOMAL SPACER; ENTEROCYTOZOON; GENETIC VARIATION; GENOTYPE; HUMANS; MICROSPORIDIOSIS; PHYLOGENY; SWINE; SWINE DISEASES;

ANIMALIA; AVES; BOS; ENTEROCYTOZOON; ENTEROCYTOZOON BIENEUSI; MICROSPORIDIA; SUIDAE; VERTEBRATA;

EID: 77952257681     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03026-09     Document Type: Article

References (66)

1. Abe, N., I. Kimata, and M. Iseki. 2009. Molecular evidence of Enterocytozoon bieneusi in Japan. J. Vet. Med. Sci. 71: 217-219.
2. Adl, S. M., A. G. Simpson, M. A. Farmer, R. A. Andersen, O. R. Anderson, J. R. Barta, S. S. Bowser, G. Brugerolle, R. A. Fensome, S. Fredericq, T. Y. James, S. Karpov, P. Kugrens, J. Krug, C. E. Lane, L. A. Lewis, J. Lodge, D. H. Lynn, D. G. Mann, R. M. McCourt, L. Mendoza, O. Moestrup, S. E. Mozley-Standridge, T. A. Nerad, C. A. Shearer, A. V. Smirnov, F. W. Spiegel, and M. F. Taylor. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52: 399-451.
3. Bandelt, H. J., P. Forster, and A. Rohl. 1999. Median-joining networks for inferring intraspecific phytogenies. Mol. Biol. Evol. 16: 37-48.
4. Bornay-Llinares, F. J., A. J. da Silva, H. Moura, D. A. Schwartz, G. S. Visvesvara, N. J. Pieniazek, A. Cruz-López, P. Hernández-Jauregui, J. Guerrero, and F. J. Enríquez. 1998. Immunologic, microscopic, and molecular evidence of Encephalitozoon intestinalis (Septata intestinalis) infection in mammals other than humans. J. Infect. Dis. 178: 820-826.
5. Breitenmoser, A. C., A. Mathis, E. Bürgi, R. Weber, and P. Deplazes. 1999. High prevalence of Enterocytozoon bieneusi in swine with four genotypes that differ from those identified in humans. Parasitology 118: 447-453.
6. Breton, J., E. Bart-Delabesse, S. Biligui, A. Carbone, X. Seiller, M. OkomeNkoumou, C. Nzamba, M. Kombila, I. Accoceberry, and M. Thellier. 2007. New highly divergent rRNA sequence among biodiverse genotypes of Enterocytozoon bieneusi strains isolated from humans in Gabon and Cameroon. J. Clin. Microbiol. 45: 2580-2589.
7. Buckholt, M. A., J. H. Lee, and S. Tzipori. 2002. Prevalence of Enterocytozoon bieneusi in swine: an 18-month survey at a slaughterhouse in Massachusetts. Appl. Environ Microbiol. 68: 2595-2599.
8. Cama, V. A., J. Pearson, L. Cabrera, L. Pacheco, R. Gilman, S. Meyer, Y. Ortega, and L. Xiao. 2007. Transmission of Enterocytozoon bieneusi between a child and guinea pigs. J. Clin. Microbiol. 45: 2708-2710.
9. Canning, E., and J. Lorn. 1986. The microsporidia of vertebrates. Academic Press, San Diego, CA.
10. Chalifoux, L. V., A. Carville, D. Pauley, B. Thompson, A. A. Lackner, and K. G. Mansfield. 2000. Enterocytozoon bieneusi as a cause of proliferative serositis in simian immunodeficiency virus-infected immunodeficient macaques (Macaca mulatta). Arch. Pathol. Lab. Med. 124: 1480-1484.
11. del Águila, C., R. Navajas, D. Gurbindo, J. T. Ramos, M. J. Mellado, S. Fenoy, M. A. Muñoz Fernández, M. Subirats, J. Ruiz, and N. J. Pieniazek. 1997. Microsporidiosis in HIV-positive children in Madrid (Spain). J. Eukaryot. Microbiol. 44: 84S-85S.
12. del Águila, C., G. P. Croppo, H. Moura, A. J. Da Silva, G. J. Leiten, D. M. Moss, S. Wallace, S. B. Slemenda, N. J. Pieniazek, and G. S. Visvesvara. 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.
13. del Águila, C., F. Izquierdo, R. Navajas, N. J. Pieniazek, G. Miró, A. I. Alonso, A. J. Da Silva, and S. Fenoy. 1999. Enterocytozoon bieneusi in animals: rabbits and dogs as new hosts. J. Eukaryot. Microbiol. 46: 8S-9S.
14. Dengjel, B., M. Zahler, W. Hermanns, K. Heinritzi, T. Spillmann, A. Thornsenke, T. Löscher, R. Gothe, and H. Rinder. 2001. Zoonotic potential of Enterocytozoon bieneusi. J. Clin. Microbiol. 39: 4495-4499.
15. Deplazes, P., A. Mathis, C. Müller, and R. Weber. 1996. Molecular epidemiology of Encephalitozoon euniculi and first detection of Enterocytozoon bieneusi in faecal samples of pigs. J. Eukaiyot. Microbiol. 43: 93S.
16. Didier, E. S. 2005. Microsporidiosis: an emerging and opportunistic infection in humans and animals. Acta Trop. 94: 61-76.
17. Didier, E. S., P. J. Didier, K. F. Snowden, and J. A. Shadduck. 2000. Microsporidiosis in mammals. Microbes Infect. 2: 709-720.
18. Didier, E. S., M. E. Stovall, L. C. Green, P. J. Brindley, K. Sestak, and P. J. Didier. 2004. Epidemiology of microsporidiosis: sources and modes of transmission. Vet. Parasitol. 126: 145-166.
19. Didier, E. S., C. R. Vossbrinck, M. D. Baker, L. B. Rogers, D. C. Bertucci, and J. A. Shadduck. 1995. Identification and characterization of three Encephalitozoon euniculi strains. Parasitology 111: 411-421.
20. Didier, E. S., and L. M. Weiss. 2006. Microsporidiosis: current status. Curr. Opin. Infect. Dis. 19: 485-492.
21. Espern, A., F. Morio, M. Miegeville, H. Illa, M. Abdoulaye, V. Meyssonnier, E. Adehossi, A. Lejeune, P. D. Cam, B. Besse, and F. Gay-Andrieu. 2007. Molecular study of microsporidiosis due to Enterocytozoon bieneusi and Encephalitozoon intestinalis among human immunodeficiency virus-infected patients from two geographical areas: Niamey, Niger, and Hanoi, Vietnam. J. Clin. Microbiol. 45: 2999-3002.
22. Excoffier, L., G. Laval, and S. Schneider. 2005. ARLEQUIN ver. 3. 0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1: 47-50.
23. Fayer, R., M. Santfn, and J. M. Trout. 2007. Enterocytozoon bieneusi in mature dairy cattle on farms in the eastern United States. Farasitol. Res. 102: 15-20.
24. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.
25. Haro, M., C. del Águila, S. Fenoy, and N. Henriques-Gil. 2003. Intraspecies genotype variability of the microsporidian parasite Encephalitozoon hellem. J. Clin. Microbiol. 41: 4166-4171.
26. Haro, M., F. Izquierdo, N. Henriques-Gil, I. Andrés, F. Alonso, S. Fenoy, and C. del Águila. 2005. First detection and genotyping of human-associated microsporidia in pigeons from urban parks. Appl. Environ. Microbiol. 71: 3153-3157.
27. Huelsenbeck, J. P., and F. Ronquist. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
28. Keeling, P. J., and C. H. Slamovits. 2004. Simplicity and complexity of microsporidian genomes. Eukaryot. Cell 3: 1363-1369.
29. Keeling, P. J., and C. H. Slamovits. 2005. Causes and effects of nuclear genome reduction. Curr. Opin. Genet. Dev. 15: 601-608.
30. Keeling, P. J., N. M. Fast, J. S. Law, B. A. Williams, and C. H. Slamovits. 2005. Comparative genomics of microsporidia. Folia Farasitol. (Fraha) 52: 8-14.
31. Keohane, E. M., and L. M. Weiss. 1998. Characterization and function of the microsporidian polar tube: a review. Folia Farasitol. (Fraha) 45: 117-127.
32. Lee, J. H. 2007. Prevalence and molecular characteristics of Enterocytozoon bieneusi in cattle in Korea. Parasito!. Res. 101: 391-396.
33. Leelayoova, S., I. Subrungruang, R. Rangsin, P. Chavalitshewinkoon- Petmitr, J. Worapong, T. Naaglor, and M. Mungthin. 2005. Transmission of Enterocytozoon bieneusi genotype a in a Thai orphanage. Am. J. Trop. Med. Hyg. 73: 104-107.
34. Leelayoova, S., I. Subrungruang, Y. Suputtamongkol, J. Worapong, P. C. Petmitr, and M. Mungthin. 2006. Identification of genotypes of Enterocytozoon bieneusi from stool samples from human immunodeficiency virusinfected patients in Thailand. J. Clin. Microbiol. 44: 3001-3004.
35. Liguory, O., C. Sarfati, F. Derouin, and J. M. Molina. 2001. Evidence of different Enterocytozoon bieneusi genotypes in patients with and without human immunodeficiency virus infection. J. Clin. Microbiol. 39: 2672-2674.
36. Lobo, M. L., L. Xiao, V. Cama, N. Magalhães, F. Antunes, and O. Matos. 2006. Identification of potentially human-pathogenic Enterocytozoon bieneusi genotypes in various birds. Appl. Environ Microbiol. 72: 7380-7382.
37. Lobo, M. L., L. Xiao, V. Cama, T. Stevens, F. Antunes, and O. Matos. 2006. Genotypes of Enterocytozoon bieneusi in mammals in Portugal. J. Eukaryot. Microbiol. 53: S61-S64.
38. López-Vélez, R., M. C. Tumentes, C. Garron, P. Montilla, R. Navajas, S. Fenoy, and C. del Águila. 1999. Microsporidiosis in travelers with diarrhea from the tropics. J. Travel Med. 6: 223-227.
39. Lores, B., C. del Águila, and C. Arias. 2002. Enterocytozoon bieneusi (Microsporidia) in faecal samples from domestic animals from Galicia, Spain. Mem. Inst. Oswaldo Cruz 97: 941-945.
40. Lores, B., I. Lápez-Miragaya, C. Arias, S. Fenoy, J. Torres, and C. del Águila. 2002. Intestinal microsporidiosis due to Enterocytozoon bieneusi in elderly human immunodeficiency virus-negative patients from Vigo, Spain. Clin. Infect. Dis. 34: 918-921.
41. Mathis, A., A. C. Breitenmoser, and P. Deplazes. 1999. Detection of new Enterocytozoon genotypes in faecal samples of farm dogs and a cat. Parasite 6: 189-193. (Pubitemid 129560720)
42. Müller, M. G., J. Kinne, R. K. Schuster, and J. Walochnik. 2008. Outbreak of microsporidiosis caused by Enterocytozoon bieneusi in falcons. Vet. Farasitol. 152: 67-78.
43. Page, R. D. M. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12: 357-358.
44. Reetz, J., H. Rinder, A Thomschke, H. Manke, M. Schwebs, and A. Bruderek. 2002. First detection of the microsporidium Enterocytozoon bieneusi in non-mammalian hosts (chickens). Int. J. Parasitol. 32: 785-787. (Pubitemid 34615871)
45. Rinder, H., S. Katzwinkel-Wladarsch, and T. Loscher. 1997. Evidence for the existence of genetically distinct strains of Enterocytozoon bieneusi. Farasitol. Res. 83: 670-672.
46. Rinder, H., A. Thomschke, B. Dengjel, R. Gothe, T. Loscher, and M. Zahler. 2000. Close genotypic relationship between Enterocytozoon bieneusi from humans and pigs and first detection in cattle. J. Parasitol. 86: 185-188. (Pubitemid 30126499)
47. Rozas, J., J. C. Sánchez-DelBarrio, X. Messeguer, and R. Rozas. 2003. DNASF, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497. (Pubitemid 38016658)
48. Sadler, F., N. Peake, R. Borrow, P. L. Rowl, E. G. Wilkins, and A. Curry. 2002. Genotyping of Enterocytozoon bieneusi in AIDS patients from the north west of England. J. Infect. 44: 39-42.
49. Santfn, M., J. A. Cortes Vecino, and R. Fayer. 2008. Enterocytozoon bieneusi genotypes in dogs in Bogota, Colombia. Am. J. Trop. Med. Hyg. 79: 215-217.
50. Santin, M., and R. Fayer. 2009. Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. J. Eukaryot. Microbiol. 56: 34-38.
51. Santín, M., J. M. Trout, and R. Fayer. 2005. Enterocytozoon bieneusi genotypes in dairy cattle in the eastern United States. Farasitol. Res. 97: 535-538.
52. Santfn, M., J. M. Trout, J. A Vecino, J. P. Dubey, and R. Fayer. 2006. Cryptosporidium, Giardia and Enterocytozoon bieneusi in cats from Bogota (Colombia) and genotyping of isolates. Vet. Farasitol. 141: 334-339.
53. Schmidt, H. A., K. Strimmer, M. Vingron, and A. von Haeseler. 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
54. Sulaiman, I. M., C. Bern, R. Gilman, V. Cama, V. Kawai, D. Vargas, E. Ticona, A. Vivar, and L. Xiao. 2003. A molecular biologic study of Enterocytozoon bieneusi in HIV-infected patients in Lima, Peru. J. Eukaryot. Microbiol. 50: 591-596.
55. Sulaiman, I. M., R. Fayer, A. A. Lal, J. M. Trout, F. W. Schaefer III, and L. Xiao. 2003. Molecular characterization of microsporidia indicates that wild mammals harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi. Appl. Environ. Microbiol. 69: 4495-4501.
56. Sulaiman, I. M., R. Fayer, C. Yang, M. Santin, O. Matos, and L. Xiao. 2004. Molecular characterization of Enterocytozoon bieneusi in cattle indicates that only some isolates have zoonotic potential. Farasitol. Res. 92: 328-334.
57. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595. (Pubitemid 19274682)
58. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
59. ten Hove, R. J., L. van Lieshout, M. B. Beadsworth, M. A. Pérez, K. Spee, E. C. Claas, and J. J. Verweij. 2009. Characterization of genotypes of Enterocytozoon bieneusi in immunosuppressed and immunocompetent patient groups. J. Eukaiyot. Microbiol. 56: 388-393.
60. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
61. Tumwine, J. K., A. Kekitiinwa, N. Nabukeera, D. E. Akiyoshi, M. A Buckholt, and S. Tzipori. 2002. Enterocytozoon bieneusi among children with diarrhea attending Mulago Hospital in Uganda. Am. J. Trop. Med. Hyg. 67: 299-303.
62. Vavra, J., and J. I. R. Larsson. 1999. Structure of the microsporidia, p. 7-84. In M. Wittner and L. M. Weiss (ed.), The microsporidia and microsporidiosis. ASM. Press, Washington, DC.
63. Visvesvara, G. S. 2002. In vitro cultivation of microsporidia of clinical importance. Clin. Microbiol. Rev. 15: 401-413.
64. Xiao, L., L. Li, G. S. Visvesvara, H. Moura, E. S. Didier, and A. A. LaI. 2001. Genotyping Encephalitozoon euniculi by multilocus analyses of genes with repetitive sequences. J. Clin. Microbiol. 39: 2248-2253.
65. Xu, Y., and L. M. Weiss. 2005. The microsporidian polar tube: a highly specialised invasion organelle. Int. J. Parasitol. 35: 941-953.
66. Zhu, X., M. Wittner, H. B. Tanowitz, A. Cali, and L. M. Weiss. 1994. Ribosomal RNA sequences of Enterocytozoon bieneusi, Septata intestinalis and Ameson michaelis: phylogenetic construction and structural correspondence J. Eukaryot. Microbiol. 41: 204-209.