Effective gene silencing in a microsporidian parasite associated with honeybee (Apis mellifera) colony declines

Applied and Environmental Microbiology

Volumn 76, Issue 17, 2010, Pages 5960-5964

  Paldi, Nitzan ^a   Glick, Eitan ^a   Oliva, Maayan ^a   Zilberberg, Yaron ^a   Aubin, Lucie ^a   Pettis, Jeffery ^b   Chen, Yanping ^b   Evans, Jay D ^b  

^a Beeologics Inc   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APIS MELLIFERA; CELLULAR COMPONENTS; CONTROLLED LABORATORIES; DISEASE AGENTS; DOUBLE-STRANDED RNA; GENE SILENCING; HONEYBEE COLONIES; HOST PHYSIOLOGY; HUMAN DISEASE; MICROSPORIDIA; PARASITE-; RNA INTERFERENCE; RNA SILENCING; TRANSPORTER GENES;

DISEASE CONTROL; GENETIC ENGINEERING; MACHINERY; PROTOZOA; RNA; VIRUSES;

GENE EXPRESSION;

CARRIER PROTEIN; DOUBLE STRANDED RNA; FUNGAL RNA; MESSENGER RNA;

DISEASE CONTROL; DISEASE PREVALENCE; FUNGUS; GENE EXPRESSION; GENOME; HONEYBEE; LABORATORY METHOD; PHYSIOLOGY; RNA; VIRAL DISEASE; VIRUS;

ANIMAL; ARTICLE; BEE; BIOSYNTHESIS; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; MICROBIOLOGY; NOSEMA;

ANIMALS; BEES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENE SILENCING; MEMBRANE TRANSPORT PROTEINS; NOSEMA; RNA, DOUBLE-STRANDED; RNA, FUNGAL; RNA, MESSENGER;

APIS MELLIFERA; APOIDEA; FUNGI; MICROSPORIDIA; NOSEMA; NOSEMA CERANAE; VERTEBRATA;

EID: 77956565514     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01067-10     Document Type: Article

References (40)

1. Aronstein, K., T. Pankiw, and E. Saldivar. 2006. SID-I is implicated in systemic gene silencing in the honey bee. J. Apic. Res. 45:20-24.
2. Bailey, L., and B. V. Ball. 1991. Honey bee pathology, 2nd ed. Academic Press, London, United Kingdom.
3. Cantwell, G. E. 1970. Standard methods for counting Nosema spores. Am. Bee J. 110:222-223.
4. Chen, Y. P., J. D. Evans, C. Murphy, R. Gutell, M. Zuker, D. Gundersen-Rindal, and J. S. Pettis. 2009. Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera. J. Eukaryot. Microbiol. 56:142-147. doi:10.1111/j.1550-7408.2008.00374.x.
5. Cornman, R. S., Y. P. Chen, M. C. Schatz, C. Street, Y. Zhao, B. Desany, M. Egholm, S. Hutchison, J. S. Pettis, W. I. Lipkin, and J. D. Evans. 2009. Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathog. 5:6.
6. Cox-Foster, D. L., S. Conlan, E. C. Holmes, G. Palacios, J. D. Evans, N. A. Moran, P. L. Quan, T. Briese, M. Hornig, D. M. Geiser, V. Martinson, D. van Engelsdorp, A. L. Kalkstein, A. Drysdale, J. Hui, J. Zhai, L. Cui, S. K. Hutchison, J. F. Simons, M. Egholm, J. S. Pettis, and W. I. Lipkin. 2007. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 3:283-287.
7. Ellis, J. D., and P. A. Munn. 2005. The worldwide health status of honey bees. Bee World 86:88-101.
8. Evans, J. D. 2006. Beepath: an ordered quantitative-PCR array for exploring honey bee immunity and disease. J. Invertebr. Pathol. 93:135-139.
9. Evans, J. D., Y. P. Chen, G. Di Prisco, J. Pettis, and V. Williams. 2009. Bee cups: single-use cages for honey bee experiments. J. Apic. Res. 48:300-302.
10. Finn, R. D., J. Tate, J. Mistry, P. C. Coggill, S. J. Sammut, H. R. Hotz, G. Ceric, K. Forslund, S. R. Eddy, E. L. L. Sonnhammer, and A. Bateman. 2008. The Pfam protein families database. Nucleic Acids Res. 36: D281-D288.
11. Fries, I. 2010. Nosema ceranae in European honey bees (Apis mellifera). J. Invertebr. Pathol. 103: S73-S79.
12. Fries, I., F. Feng, A. Da Silva, S. B. Slemenda, and N. J. Pieniazek. 1996. Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur. J. Protistol. 32:356-365.
13. Fries, I., R. Martin, A. Meana, P. Garcia-Palencia, and M. Higes. 2006. Natural infections of Nosema ceranae in European honey bees. J. Apic. Res. 45:230-233.
14. Higes, M., P. Garcia-Palencia, R. Martin-Hernandez, and A. Meana. 2007. Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). J. Invertebr. Pathol. 94:211-217.
15. Higes, M., R. Martin-Hernandez, C. Botias, E. G. Bailon, A. V. Gonzalez-Porto, L. Barrios, M. J. Del Nozal, J. L. Bernal, J. J. Jimenez, P. G. Palencia, and A. Meana. 2008. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 10:2659-2669.
16. Higes, M., R. Martin, and A. Meana. 2006. Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J. Invertebr. Pathol. 92:81-83.
17. Hirt, R. P., B. Healy, C. R. Vossbrinck, E. U. Canning, and T. M. Embley. 1997. A mitochondrial Hsp70 orthologue in Vairimorpha necatrix: molecular evidence that microsporidia once contained mitochondria. Curr. Biol. 7:995-998.
18. Hirt, R. P., J. M. Logsdon, Jr., B. Healy, M. W. Dorey, W. F. Doolittle, and T. M. Embley. 1999. Microsporidia are related to fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc. Natl. Acad. Sci. U. S. A. 96:580-585.
19. Honeybee Genome Sequencing Consortium. 2006. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931-949.
20. Huang, W.-F., J.-H. Jiang, Y.-W. Chen, and C.-H. Wang. 2007. A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 38:30-37.
21. Katinka, M. D., S. Duprat, E. Cornillott, G. Meteinler, F. Thomarat, G. Prensier, V. Barbe, E. Peyretaillade, P. Brottier, P. Wincker, F. Delbac, H. El Alaoul, P. Peyret, W. Saurin, M. Gouy, J. Weissenbach, and C. P. Vivares. 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450-453.
22. Keeling, P. J., M. A. Luker, and J. D. Palmer. 2000. Evidence from betatubulin phylogeny that microsporidia evolved from within the fungi. Mol. Biol. Evol. 17:23-31.
23. Keeling, P. J., and G. I. McFadden. 1998. Origins of microsporidia. Trends Microbiol. 6:19-23.
24. Klee, J., A. M. Besana, E. Genersch, S. Gisder, A. Nanetti, D. Q. Tam, T. X. Chinh, F. Puerta, J. M. Ruz, P. Kryger, D. Message, F. Hatjina, S. Korpela, I. Fries, and R. J. Paxton. 2007. Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J. Invertebr. Pathol. 96:1-10.
25. a. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, L. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
26. Letunic, I., T. Doerks, and P. Bork. 2009. SMART 6: recent updates and new developments. Nucleic Acids Res. 37: D229-D232.
27. Lipardi, C., and B. M. Paterson. 2009. Identification of an RNA-dependent RNA polymerase in Drosophila involved in RNAi and transposon suppression. Proc. Natl. Acad. Sci. U. S. A. 106:15645-15650.
28. Maori, E., N. Paldi, S. Shafir, H. Kalev, E. Tsur, E. Glick, and I. Sela. 2009. IAPV, a bee-affecting virus associated with colony collapse disorder can be silenced by dsRNA ingestion. Insect Mol. Biol. 18:55-60.
29. Mayack, C., and D. Naug. 2009. Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection. J. Invertebr. Pathol. 100:185-188.
30. Molina, J.-M., M. Tourneur, C. Sarfati, S. Chevret, A. De Gouvello, J. G. Gobert, S. Balkan, and F. Derouin. 2002. Fumagillin treatment of intestinal microsporidiosis. N. Engl. J. Med. 346:1963-1969.
31. Morse, R. A., and K. Flottum (ed.). 1997. Honey bee pests, predators and diseases, 3rd ed. A. I. Root Co., Medina, OH.
32. Siomi, H., and M. Siomi. 2009. On the road to reading the RNA-interference code. Nature 457:396-404.
33. Söding, J. 2005. Protein homology detection by HMM-HMM comparison. Bioinformatics 21:951-960.
34. Reference deleted.
35. Tsaousis, A. D., E. R. S. Kunji, A. V. Goldberg, J. M. Lucocq, R. P. Hirt, and T. M. Embley. 2008. A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453:553-556.
36. Van de Peer, Y., A. Ben Ali, and A. Meyer. 2000. Microsporidia: accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryotes are just curious fungi. Gene 246:1-8.
37. van Engelsdorp, D., J. D. Evans, C. Saegerman, C. Mullin, E. Haubruge, B. K. Nguyen, M. A. Frazier, J. Frazier, D. Cox-Foster, Y. Chen, R. Underwood, D. R. Tarpy, and J. S. Pettis. 2009. Colony collapse disorder: a descriptive study. PLoS One 4(8):e6481.
38. Waterhouse, A. M., J. B. Procter, D. M. Martin, M. Clamp, and G. J. Barton. 2009. Jalview version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189-1191.
39. Williams, G. R., M. A. Sampson, D. Shutler, and R. E. L. Rogers. 2008. Does fumagillin control the recently detected invasive parasite Nosema ceranae in western honey bees (Apis mellifera)? J. Invertebr. Pathol. 99:342-344.
40. Zdobnov, E. M., and R. Apweiler. 2001. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847-848.