International Journal of Industrial Entomology and Biomaterials

Korean Society of Sericultural Science (한국잠사학회)
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Identification, Characterization, and DNA Sequencing of Nosema bombi in Bumblebees from Gangwon Province, Korea

  • Kwak, Kyu-Won (Department of Agricultural Biology, National Academy of Agricultural Science) ;
  • Yoon, Hyung-Joo (Department of Agricultural Biology, National Academy of Agricultural Science) ;
  • Choi, Youngcheol (Department of Agricultural Biology, National Academy of Agricultural Science) ;
  • Park, Kwanho (Department of Agricultural Biology, National Academy of Agricultural Science) ;
  • Hwang, Jaesam (Department of Agricultural Biology, National Academy of Agricultural Science) ;
  • Kim, Hyunae (Department of Agricultural Biology, National Academy of Agricultural Science) ;
  • Nam, Sunghee (Department of Agricultural Biology, National Academy of Agricultural Science)
  • Received : 2013.11.07
  • Accepted : 2013.11.18
  • Published : 2013.12.31
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Abstract

The purpose of this study was to quickly and effectively identify the Nosema disease of bumblebees in Gangwon Province in Korea. Bumblebees are crucial pollinators of various crops, and microsporidia are the critical pathogens of these hosts. When bumblebees are infected with Nosema bombi, their abdomens can become distended. Paralyzed and infected workers often become sluggish and die early. We have identified the morphology of the microsporidium by light and electron microscopy, and found it to have fairly small oval spores, as has been described previously in many other articles. For the specific and sensitive diagnosis of the microsporidian parasite N. bombi in bumblebees, we have developed an improved method of the polymerase chain reaction (PCR) for expeditious diagnosis. Two pairs of primers were tested on N. bombi and the related microsporidia Nosema apis and Nosema sp., both of which infect Bombus ignitus and Bombus hypocrita sapporoensis. Furthermore, we have verified and analyzed the 16SrRNA sequence data of N. bombi in bumblebees by using the Basic Local Alignment Search Tool (BLAST) server at the National Center for Biotechnology Information.

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References

  1. Bollan KA, Hothersall JD, Moffat C, Durkacz J, Saranzewa N et al. (2013) The microsporidian parasites Nosema ceranae and Nosema apis are widespread in honeybee (Apis mellifera) colonies across Scotland. Parasitology research 112, 751-759. https://doi.org/10.1007/s00436-012-3195-0
  2. Chen YP, Evans JD, Murphy C, Gutell R, Zuker M et al. (2009) Morphological, molecular, and phylogenetic characterization of Nosema ceranae, a microsporidian parasite isolated from the European honey bee, Apis mellifera. The Journal of eukaryotic microbiology 56,142-147. https://doi.org/10.1111/j.1550-7408.2008.00374.x
  3. Choi JY, Lee ML, Nam SH, Kim JG, Choi YC, Kim WT, Sim HS, Kim KY (2006) Multiplex Polymoerase Chain Reaction Assay for Simultaneous Detection of Nosema ceranae, Ascosphaera apis and Paenibacillus larvae in Honey bee. Korean Journal of Apiculture 21, 93-100.
  4. Colla SR, Otterstatter MC, Gegear RJ, Thomson JD (2006) Plight of the bumble bee: Pathogen spillover from commercial to wild populations. Biological Conservation 129, 461-467. https://doi.org/10.1016/j.biocon.2005.11.013
  5. Flanders RV, Wehling WF, Craghead AL (2003) Laws and regulations on the import, movement and release of bees in the United States. In K. Strickler and J.H. Cane (editors), For Nonnative Crops, Whence Pollinators of the Future? Thomas Say Publications in Entomology, Lanham, MD. 99-111.
  6. Fries I (2010) Nosema ceranae in European honey bees (Apis mellifera). Journal of invertebrate pathology 103 Suppl 1, 73-79. https://doi.org/10.1016/j.jip.2009.06.017
  7. Fries I, Feng F, da Silva A, Slemenda SB, Pieniazek NJ (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. https://doi.org/10.1016/S0932-4739(96)80059-9
  8. Graystock P, Yates K, Evison SEF, Darvill B, Goulson D, Hughes W et al. (2013) The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies. Journal of Applied Ecology 1365-2664.
  9. Hylis M, Pilarska DK, Obornik M, Vavra J, Solter LF, Weiser J et al. (2006) Nosema chrysorrhoeae n. sp. (Microsporidia), isolated from browntail moth (Euproctis chrysorrhoea L.) (Lepidoptera, Lymantriidae) in Bulgaria: characterization and phylogenetic relationships. Journal of invertebrate pathology 91, 105-114. https://doi.org/10.1016/j.jip.2005.11.006
  10. Imhof B, Schumid-Hempel P (2006) Colony success of the bumble bee bombus terrestris in relation to infections by two protozoan parasites Crithidia bombi and Nosem abombi. Ecological Entomology 33, 577-582.
  11. Kaftanoglu O, Eldeniz N (2006) An investigation on some diseases and parasites of bumble bee queens in turkey. Pakistan Journal of Biological Science 9:1282-1286. [Internet]. Available from: http:// www.eco.ethz.ch/research/sociallife. https://doi.org/10.3923/pjbs.2006.1282.1286
  12. Keeling PJ, Fast NM (2002) Microsporidia: biology and evolution of highly reduced intracellular parasites. Annual review of microbiology 56, 93-116. https://doi.org/10.1146/annurev.micro.56.012302.160854
  13. Kim WT, Choi JY, Kim JG, Whang SJ, Choi YC, Han SM, Kim MA, Lee DW, Yoon HJ (2008) Isolation of Insect Pathogenic Bacteria from Bombus terrestris and B.ignitus in Korea. Korean Journal of Apiculture 23, 13-20.
  14. Kissinger CN, Cameron SA, Thorp RW, White B, Solter LF (2011) Survey of bumble bee (Bombus) pathogens and parasites in Illinois and selected areas of northern California and southern Oregon. Journal of invertebrate pathology 107, 220-224. https://doi.org/10.1016/j.jip.2011.04.008
  15. Koch JB, Strange JP (2012) The Status of Bombus occidentalisandB. moderatusin Alaska with Special Focus onNosema bombiIncidence. Northwest Science 86, 212-220. https://doi.org/10.3955/046.086.0306
  16. Larsson JI (2007) Cytological variation and pathogenicity of the bumble bee parasite Nosema bombi (Microspora, Nosematidae). Journal of invertebrate pathology 94, 1-11. https://doi.org/10.1016/j.jip.2006.07.006
  17. Moeller FE (1978) Nosema disease: its control in honey bee colonies. United States Dept of Agriculture, Technical Bulletin Number 1569, Science and Education Administration 1-15.
  18. Moon JY (1966) Gajamhaebusangli-hak, Jambyung-hak 3. Hyangmoonsa, Republic of Korea, 225-276.
  19. Li J, Chen W, Wu J, Peng W, An J, Schmid-Hempel P, Schmid-Hempel R (2012) Diversity of Nosema associated with bumblebees (Bombus spp.) from China. International journal for parasitology 42, 49-61. https://doi.org/10.1016/j.ijpara.2011.10.005
  20. Otti O, Schmid-Hempel P (2007) Nosema bombi: A pollinator parasite with detrimental fitness effects. Journal of invertebrate pathology 96, 118-124. https://doi.org/10.1016/j.jip.2007.03.016
  21. Otti O, Schmid-Hempel P (2008) A field experiment on the effect ofNosema bombiin colonies of the bumblebeeBombus terrestris. Ecological Entomology 33, 577-582. https://doi.org/10.1111/j.1365-2311.2008.00998.x
  22. Schmid-Hempel P (2001) On the evolutionary ecology of host-parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88, 147-158. https://doi.org/10.1007/s001140100222
  23. Schmid-Hempel P, Loosli R (1998) A contribution of the knowledge of nosema infections in bumble bees, bombus spp. Apidologie 29, 525- 535. https://doi.org/10.1051/apido:19980605
  24. Shafer AB, Williams GR, Shutler D, Rogers RE, Stewart DT (2009) Cophylogeny of Nosema (Microsporidia: Nosematidae) and bees (Hymenoptera: Apidae) suggests both cospeciation and a host-switch. The Journal of parasitology 95, 198-203. https://doi.org/10.1645/GE-1724.1
  25. Tanada Y, Kaya HK (1994) Insect Pathology. Academic Press INC. Harcourt Brace Jovanovich, Pubrichers, San Diego. [Internet]. Available from: http://wiki.ceh.ac.uk [accessed on 27 October 2013].
  26. Velthuis HHW, van Doorn A (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37, 421- 451. https://doi.org/10.1051/apido:2006019
  27. Vossbrink CR, Debrunner-Vossbrink BA (2005) Molecular Phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitologica 52, 131-142. https://doi.org/10.14411/fp.2005.017
  28. Weiser J (1961) Die Mikrosporidien als Parasiten der Insekten. Monographien zur angewandte Entomologie 17. Verlag Paul Parey, Hamburg und Berlin.
  29. Whittington R, Winston ML (2003) Effects of Nosema bombi and its treatment fumagillin on bumble bee (Bombus occidentalis) colonies. Journal of invertebrate pathology 84, 54-58. https://doi.org/10.1016/S0022-2011(03)00123-X
  30. Yoo MS, Kim IW, Kang MH, Han SH,Yoon BS (2008) Development of Real-Time PCR Mehod for the Detection of Nosema. Korean Journal of Apiculture 23, 241-249.
  31. Zhang Y, Ding J, Yu G, Su G (1996) The relationship of pebrine of Antheraca perny and filed insects. LiaoNing Agric. Sci. 5, 31-34. [Internet]. Available from : http://www.silkpathdb.swu.edu.cn.png [accessed on 27 October 2013].
  32. Zhu F, Shen Z, Guo X, Xu X, Tao H, Tang X, Xu L (2011) A new isolate of Nosema sp. (Microsporidia, Nosematidae) from Phyllobrotica armata Baly (Coleoptera, Chrysomelidae) from China. Journal of invertebrate pathology 106, 339-342. https://doi.org/10.1016/j.jip.2010.10.005

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