Complete rRNA gene sequences reveal that the microsporidium Nosema bombi infects diverse bumblebee (Bombus spp.) hosts and contains multiple polymorphic sites

Journal of Eukaryotic Microbiology

Volumn 52, Issue 6, 2005, Pages 505-513

  Tay, Wee Tek ^a,b   O'Mahony, Elaine M ^a   Paxton, Robert J ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

(GTTT) repeat unit; Indel; Internal transcribed spacer; Large subunit; Microsporidia; Small subunit; SNP

Indexed keywords

BEE; DNA; FUNGAL DISEASE; FUNGUS; GENE EXPRESSION; GENETIC DIFFERENTIATION; HOST-PATHOGEN INTERACTION; POLYMORPHISM; RNA;

EURASIA; EUROPE;

MICROSPORIDIA; MICROSPORIDIUM; MICROSPORUM; NOSEMA; NOSEMA BOMBI;

FUNGAL DNA; RIBOSOMAL SPACER DNA;

ANIMAL; ARTICLE; BEE; CLASSIFICATION; DNA SEQUENCE; GENETIC VARIABILITY; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; NOSEMA; NUCLEOTIDE SEQUENCE; PATHOGENICITY; RNA GENE; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; BASE SEQUENCE; BEES; DNA, FUNGAL; DNA, RIBOSOMAL SPACER; GENES, RRNA; MOLECULAR SEQUENCE DATA; NOSEMA; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ANALYSIS, DNA; VARIATION (GENETICS);

EID: 31944451549     PISSN: 10665234     EISSN: 15507408     Source Type: Journal    
DOI: 10.1111/j.1550-7408.2005.00057.x     Document Type: Article

References (60)

1. Arnheim, N. 1983. Concerted evolution of multigene families. In: Nei, M. & Koehn, R. K. (ed.), Evolution of Genes and Proteins. Sinauer, Sunderland, MA. p. 38-61.
2. Aytekín, A. M., Çagatay, N. & Hazir, S. 2002. Floral choices, parasites and micro-organisms in natural populations of bumblebees (Apidae: Hymenoptera) in Ankara province. Turk. J. Zool., 26:149-155.
3. Beebee, T. & Rowe, G. 2004. An Introduction to Molecular Ecology. Oxford University Press, Oxford, UK. 346 p.
4. Bell, A. S. & Ranford-Cartwright, L. C. 2002. Real-time quantitative PCR in parasitology. Trends Parasitol., 18:337-342.
5. Bell, A. S., Aoki, T. & Yokoyama, H. 2001. Phylogenetic relations among Microsporidia based on rDNA sequence data, with particular reference to fish-infecting Microsporidium Balbiani 1884 species. J. Eukaryot. Microbiol., 48:258-265.
6. Biderre, C., Duffieux, F., Peyretaillade, E., Glaser, P., Peyret, P., Danchin, A., Pagès, M., Méténier, G. & Vivarès, C. P. 1997. Mapping of repetitive and non-repetitive DNA probes to chromosomes of the microsporidian Encephalitozoon cuniculi. Gene, 191:39-45.
7. Brown, G. D., Hudson, K. L. & Reece, K. S. 2004. Multiple polymorphic sites at the ITS and ATAN loci in cultured isolates of Perkinsus marinus. J. Eukaryot. Microbiol., 51:312-320.
8. Brown, S. P., Hochberg, M. E. & Grenfell, B. T. 2002. Does multiple infection select for raised virulence? Trends Microbiol., 10:401-405.
9. Brugère, J.-F., Cornillot, E., Méténier, G., Bensimon, A. & Vivarès, C. P. 2000. Encephalitozoon cuniculi (Microspora) genome: physical map and evidence for telomere-associated rDNA units on all chromosomes. Nucleic Acids Res., 28:2026-2033.
10. Canning, E. U., Refardt, D., Vossbrinck, C. R., Okamura, B. & Curry, A. 2002. New diplokaryotic microsporidia (Phylum Microsporidia) from freshwater bryozoans (Bryozoa, Phylactolaemata). Eur. J. Protistol., 38:247-265.
11. Canning, E. U., Curry, A., Cheney, S. A., Lafranchi-Tristem, N. J., Kawakami, Y., Hatakeyama, Y., Iwano, H. & Ishihara, R. 1999. Nosema tyriae n. sp. and Nosema sp. Microspridian parasites of Cinnabar moth Tyria jacobaeae. J. Invert. Pathol., 74:29-38.
12. Chao, L., Hanley, K. A., Burch, C. L., Dahlberg, C. & Turner, P. E. 2000. Kin selection and parasite evolution: higher and lower virulence with hard and soft selection. Q. Rev. Biol., 75:261-275.
13. Cheesman, S. J., de Roode, J. C., Read, A. F. & Carter, R. 2003. Real-time quantitative PCR for analysis of genetically mixed infections of malaria parasites: technique validation and applications. Mol. Biochem. Parasitol., 131:83-91.
14. Cline, J., Braman, J. C. & Hogrefe, H. H. 1996. PCR fidelity of Pfu DNA polymerase and other thermostable DNA polymerases. Nucleic Acids Res., 24:3546-3551.
15. Colgan, D. J. 1993. DNA regeneration in the Polymerase Chain Reaction. J. Theor. Biol., 162:289-307.
16. Dahllöf, I., Baillie, H. & Kjelleberg, S. 2000. rpoB-based microbial community analysis avoids limitations inherent in 16S rRNA gene intraspecies heterogeneity. Appl. Environ. Microb., 66:3376-3380.
17. Didier, E. S., Vossbrinck, C. R., Baker, M. D., Rogers, L. B., Bertucci, D. C. & Shadduck, J. A. 1995. Identification and characterization of three Encephalitozoon cuniculi strains. Parasitology, 111:411-421.
18. Dover, G. 1982. Molecular drive: a cohesive mode of species evolution. Nature, 299:111-117.
19. Dover, G. & Coen, E. 1981. Springcleaning ribosomal DNA: a model for multigene evolution? Nature, 290:731-732.
20. Duran, S., Giribet, G. & Turon, X. 2004. Phylogeographical history of the sponge Crambe crambe (Porifera, Poecilosclerida): range expansion and recent invasion of the Macaronesian islands from the Mediterranean Sea. Mol. Ecol., 13:109-122.
21. Durrer, S. & Schmid-Hempel, P. 1995. Parasites and the regional distribution of bumble bee species. Ecography, 18:114-122.
22. Frank, S. A. 1996. Models of parasite virulence. Q. Rev. Biol., 71:37-78.
23. Fries, I., Feng, F., da Silva, A., Slemenda, S. B. & Pieniazek, N. J. 1996. Nosema ceranae n. sp. (Micropsora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur. J. Protistol., 32:356-365.
24. Fries, I., De Ruijter, A., Paxton, R. J., da Silva, A. J., Slemenda, S. B. & Pieniazek, N. J. 2001. Molecular characterization of Nosema bombi (Microsporidia: Nosematidae) and a note on its sites of infection in Bombus terrestris (Hymenoptera: Apoidea). J. Apicult. Res., 40:91-96.
25. Gatehouse, H. S. & Malone, L. A. 1998. The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence of small and large subunit rRNA genes and evidence of a large tandem repeat unit size. J. Invert. Pathol., 71:97-105.
26. Goka, K., Okabe, K., Yoneda, M. & Niwa, S. 2001. Bumblebee commercialization will cause worldwide migration of parasitic mites. Mol. Ecol., 10:2095-2099.
27. Guscetti, F., Mathis, A., Halt, J. M. & Deplazes, P. 2003. Overt fatal and chronic subclinical Encephalitozoon cuniculi microsporidiosis in a colony of captive emperor tamarins (Saguinus imperator). J. Med. Primatol., 32:111-119.
28. Katinka, M. D., 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, C. P. 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature, 414:450-453.
29. Kawakami, Y., Inoue, T., Ito, T., Kitamisu, K., Hanawa, C., Ando, T., Iwano, H. & Ishihara, R. 1994. Identification of a chromosome harbouring the small sub-unit ribosomal RNA gene of Nosema bombycis. J. Invert. Pathol., 64:147-148.
30. Keeling, P. J. & Fast, N. M. 2002. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu. Rev. Microbiol., 56:93-116.
31. Kumar, S., Tamura, K. & Nei, M. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform., 5:150-163.
32. Liu, S., Thaler, D. S. & Libchaber, A. 2002. Signal and noise in bridging PCR. BMC Biotechnol., 2:13.
33. Lom, J., Nilsen, F. & Dyková, I. 2001. Thelohania contejeani Henneguy, 1982: dimorphic life cycle and taxonomic affinities, as indicated by ultrastructural and molecular study. Parasitol. Res., 87:860-872.
34. MacFarlane, R. P., Lipa, J. J. & Liu, H. J. 1995. Bumble bee pathogens and internal enemies. Bee World, 76:130-148.
35. Massey, R. C., Buckling, A. & ffrench-Constant, R. 2004. Interference competition and parasite virulence. Proc. R. Soc. Ser. B - Biol., 271:785-788.
36. Mathis, A., Åkerstedt, J., Tharaldsen, J., Ødegaard, Ø. & Deplazes, P. 1996. Isolates of Encephalitozoon cuniculi from farmed blue foxes (Alopex lagopus) from Norway differ from isolates from Swiss domestic rabbits (Oryctolagus cuniculus). Parasitol. Res., 82:727-730.
37. McIvor, C. A. & Malone, L. A. 1995. Nosema bombi, a microsporidian pathogen of the bumble bee Bombus terrestris (L.). NZ J. Zool., 22:25-31.
38. Mohra, C., Fellendorf, M., Segelbacher, G. & Paxton, R. J. 2000. Dinucleotide microsatellite loci for Andrena vaga and other andrenid bees from non-enriched and CT-enriched libraries. Mol. Ecol., 9:2189.
39. Moser, B. A., Becnel, J. J. & Williams, D. F. 2000. Morphological and molecular characterization of the Thelohania solenopsae complex (Microsporidia: Thelohaniidae). J. Invert. Pathol., 75:174-177.
40. Parkin, E. J. & Butlin, R. K. 2004. Within- and between-individual sequence variation among ITS1 copies in the meadow grasshopper Chorthippus parallelus indicates frequent intrachromosomal gene conversion. Mol. Biol. Evol., 21:1595-1601.
41. Pecher, W. T., Robledo, J. A. F. & Vasta, G. R. 2004. Identification of a second rRNA gene unit in the Perkinsus andrewsi genome. J. Eukaryot. Microbiol., 51:234-245.
42. Prys-Jones, O. E. & Corbet, S. A. 1987. Bumblebees. Cambridge University Press, Great Britain. 86 p.
43. Schmid-Hempel, P. & Loosli, R. 1998. A contribution to the knowledge of Nosema infections in bumble bees, Bombus spp. Apidologie, 29: 525-535.
44. Shykoff, J. A. & Schmid-Hempel, P. 1991. Incidence and effects of four parasites in natural populations of bumble bees in Switzerland. Apidologie, 22:117-125.
45. Slamovits, C. H., Williams, B. A. & Keeling, P. J. 2004. Transfer of Nosema locustae (Microsporidia) to Antonospora locustae n. comb. based on molecular and ultrastructural data. J. Eukaryot. Microbiol., 51:207-213.
46. Sokolova, Y. Y., McNally, L. R., Fuxa, J. R. & Vinson, S. B. 2004. Spore morphotypes of Thelohania solenopsae (microsporidia) described microscopically and confirmed by PCR of individual spores microdissected from smears by position ablative laser microbeam microscopy. Microbiology, 150:1261-1270.
47. Solter, L. F. & Maddox, J. V. 1998. Physiological host specificity of microsporidia as an indicator of ecological host specificity. J. Invert. Pathol., 71:207-216.
48. Solter, L. F., Siegel, J. P., Pilarska, D. K. & Higgs, M. C. 2002. The impact of mixed infection of three species of microsporidian isolated from the gypsy moth Lymantria dispar L. (Lepidoptera:Lymantriidae). J. Invert. Pathol., 81:103-113.
49. Staden, R., Beal, K. F. & Bonfield, J. K. 2000. The Staden package, 1998. Methods Mol. Biol., 132:115-130.
50. Thompson, J. D., Higgins, D. G. & Gibson, T. J. 1994. CLUSTAL W: improving the sensitivity of progressing multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22:4673-4680.
51. Tsai, S.-J., Lo, C.-F., Soichi, Y. & Wang, C.-H. 2003. The characterization of microsporidian isolates (Nosematidae: Nosema) from five important lepidopteran pests in Taiwan. J. Invert. Pathol., 83:51-59.
52. van Doorn, A. & Velthuis, H. 2004. Developments in breeding, commercialization and economic value of bumblebees. In: Bernardinelli, I. & Milani, N. (ed.), Proceedings of the First European Conference of Apidology. Udine, Italy, September 2004. p. 71.
53. Vanhoutte, T., Huys, G., De Brandt, E. & Swings, J. 2004. Temporal stability analysis of the microbiota in human feces by denaturing gradient gel electrophoresis using universal and group-specific 16S rRNA gene primers. FEMS Microbiol. Ecol., 48:437-446.
54. Vivarès, C. P. 2001. Introduction: the "microsporidial world", a paragon for analysing intracellular parasitism. Microbes Infect., 3:371-372.
55. Vivarès, C. P., Gouy, M., Thomara, F. & Mété nier, G. 2002. Functional and evolutionary analysis of a eukaryotic parasitic genome. Curr. Opin. Microbiol., 5:499-505.
56. Walsh, P. S., Metzger, D. A. & Higuchi, R. 1991. Chelex® 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques, 10:507.
57. Whittington, R. & Winston, M. L. 2003. Effects of Nosema bombi and its treatment fumagillin on bumble bee (Bombus occidentalis) colonies. J. Invert. Pathol., 84:54-58.
58. Williams, P. H. 1998. An annotated checklist of bumble bees with an analysis of patterns of description (Hymenoptera: Apidae, Bombini). Bull. Nat. Hist. Museum (Entomol.), 67:79-152.
59. Wittner, M. & Weiss, L. M. 1999. The Microsporidia and Microsporidosis. ASM Press, Washington, DC. 553 p.
60. Xiao, L., Li, L., Visvesvara, G. S., Moura, H., Didier, E. S. & Lal, A. A. 2001. Genotyping Encephalitozoon cuniculi by multilocus analyses of genes with repetitive sequences. J. Clin Microbiol., 39:2248-2253.