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High levels of genetic diversity in Nosema ceranae within Apis mellifera colonies

Published online by Cambridge University Press:  15 November 2013

TAMARA GÓMEZ-MORACHO ,
XULIO MASIDE ,
RAQUEL MARTÍN-HERNÁNDEZ ,
MARIANO HIGES  and
CAROLINA BARTOLOMÉ
TAMARA GÓMEZ-MORACHO*
Affiliation:
Laboratorio de Patología Apícola, Centro Apícola Regional, JCCM, 19180 Marchamalo, Spain
XULIO MASIDE
Affiliation:
Departamento de Anatomía Patolóxica e Ciencias Forenses, Universidade de Santiago de Compostela, 15782 Santiago de Compostela, Galicia, Spain Grupo de Medicina Xenómica, CIMUS, Universidade de Santiago de Compostela, 15782 Santiago de Compostela, Galicia, Spain Grupo de Xenómica Comparada de Parásitos Humanos, IDIS, Santiago de Compostela, Galicia, Spain
RAQUEL MARTÍN-HERNÁNDEZ
Affiliation:
Laboratorio de Patología Apícola, Centro Apícola Regional, JCCM, 19180 Marchamalo, Spain Instituto de Recursos Humanos para la Ciencia y la Tecnología (INCRECYT), Fundación Parque Científico Tecnológico de Albacete, Spain
MARIANO HIGES
Affiliation:
Laboratorio de Patología Apícola, Centro Apícola Regional, JCCM, 19180 Marchamalo, Spain
CAROLINA BARTOLOMÉ
Affiliation:
Departamento de Anatomía Patolóxica e Ciencias Forenses, Universidade de Santiago de Compostela, 15782 Santiago de Compostela, Galicia, Spain Grupo de Medicina Xenómica, CIMUS, Universidade de Santiago de Compostela, 15782 Santiago de Compostela, Galicia, Spain Grupo de Xenómica Comparada de Parásitos Humanos, IDIS, Santiago de Compostela, Galicia, Spain
*
*Corresponding author: Camino de San Martín sn. 19180, Marchamalo, Spain. E-mail: [email protected]
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Summary

Nosema ceranae is a widespread honeybee parasite, considered to be one of the pathogens involved in the colony losses phenomenon. To date, little is known about its intraspecific genetic variability. The few studies on N. ceranae variation have focused on the subunits of ribosomal DNA, which are not ideal for this purpose and have limited resolution. Here we characterized three single copy loci (Actin, Hsp70 and RPB1) in three N. ceranae isolates from Hungary and Hawaii. Our results provide evidence of unexpectedly high levels of intraspecific polymorphism, the coexistence of a wide variety of haplotypes within each bee colony, and the occurrence of genetic recombination in RPB1. Most haplotypes are not shared across isolates and derive from a few frequent haplotypes by a reduced number of singletons (mutations that appear usually just once in the sample), which suggest that they have a fairly recent origin. Overall, our data indicate that this pathogen has experienced a recent population expansion. The presence of multiple haplotypes within individual isolates could be explained by the existence of different strains of N. ceranae infecting honeybee colonies in the field which complicates, and must not be overlooked, further analysis of host–parasite interactions.

Keywords

Nosema ceranaeActinHsp70RPB1genetic diversity
Type
Research Article
Information
Parasitology , Volume 141 , Issue 4 , April 2014 , pp. 475 - 481
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Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Botías, C., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A., Martínez-Salvador, A., De la Rúa, P., Meana, A. and Higes, M. (2012). The growing prevalence of Nosema ceranae in honey bees in Spain, an emerging problem for the last decade. Research in Veterinary Science 93, 150–155. doi: 10.1016/j.rvsc.2011.08.002.CrossRefGoogle ScholarPubMed
Botías, C., Martín-Hernández, R. and Barrios, L. (2013). Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Veterinary Research 44, 25. doi: 10.1186/1297-9716-44-25.CrossRefGoogle ScholarPubMed
Chaimanee, V., Chen, Y.-P. Y., Pettis, J. S., Scott Cornman, R. and Chantawannakul, P. (2011). Phylogenetic analysis of Nosema ceranae isolated from European and Asian honeybees in Northern Thailand. Journal of Invertebrate Pathology 107, 229–233. doi: 10.1016/j.jip.2011.05.012.CrossRefGoogle ScholarPubMed
Cornman, R. S., Chen, Y. P., Schatz, M. C., Street, C., Zhao, Y., Desany, B., Egholm, M., Hutchison, S., Pettis, J. S., Lipkin, W. I. and Evans, J. D. (2009). Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathogens 5, e1000466. doi: 10.1371/journal.ppat.1000466.CrossRefGoogle ScholarPubMed
Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L. and Neumann, P. (2012 a). Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Applied and Environmental Microbiology 78, 981–987. doi: 10.1128/AEM.06537-11.CrossRefGoogle ScholarPubMed
Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L. and Neumann, P. (2012 b). Predictive markers of honey bee colony collapse. PLoS ONE 7, e32151. doi: 10.1371/journal.pone.0032151.CrossRefGoogle ScholarPubMed
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797. doi: 10.1093/nar/gkh340.CrossRefGoogle ScholarPubMed
Fries, I., Feng, F., Da Silva, A., Slemenda, S. B. and Pieniazek, N. (1996). Nosema ceranae n.sp (Microspora: Nosematidae), morphological and molecular characterization of a Microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera: Apidae). European Journal of Protistology 32, 356–365.CrossRefGoogle Scholar
Fu, Y. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.CrossRefGoogle ScholarPubMed
Genersch, E. (2010). Honey bee pathology: current threats to honey bees and beekeeping. Applied Microbiology and Biotechnology 87, 87–97. doi: 10.1007/s00253-010-2573-8.CrossRefGoogle ScholarPubMed
Hall, T. A. (1999). Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hatjina, F., Tsoktouridis, G., Bouga, M., Charistos, L., Evangelou, V., Avtzis, D., Meeus, I., Brunain, M., Smagghe, G. and De Graaf, D. C. (2011). Polar tube protein gene diversity among Nosema ceranae strains derived from a Greek honey bee health study. Journal of Invertebrate Pathology 108, 131–134. doi: 10.1016/j.jip.2011.07.003.CrossRefGoogle ScholarPubMed
Higes, M., Martín, R. and Meana, A. (2006). Nosema ceranae, a new microsporidian parasite in honeybees in Europe. Journal of Invertebrate Pathology 92, 93–95. doi: 10.1016/j.jip.2006.02.005.CrossRefGoogle ScholarPubMed
Higes, M., Martín-Hernández, R. and Meana, A. (2010). Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 41, 375–392. doi: 10.1051/apido/2010019.CrossRefGoogle Scholar
Higes, M., Meana, A., Bartolomé, C., Botías, C. and Martín-Hernández, R. (2013). Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environmental Microbiology Reports 5, 17–29. doi: 10.1111/1758-2229.12024.CrossRefGoogle ScholarPubMed
Hirt, R. P., Logsdon, J. M., Healy, B., Dorey, M. W., Doolittle, W. F. and Embley, T. M. (1999). Microsporidia are related to fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proceedings of the National Academy of Sciences USA 96, 580–585. doi: 10.1073/pnas.96.2.580.CrossRefGoogle ScholarPubMed
Huang, Q., Kryger, P., Le Conte, Y. and Moritz, R. F. (2012). Survival and immune response of drones of a Nosemosis tolerant honey bee strain towards N. ceranae infections. Journal of Invertebrate Pathology 109, 297–302. doi: 10.1016/j.jip.2012.01.004.CrossRefGoogle ScholarPubMed
Huang, W.-F., Bocquet, M., Lee, K.-C., Sung, I.-H., Jiang, J.-H., Chen, Y.-W. and Wang, C.-H. (2008). The comparison of rDNA spacer regions of Nosema ceranae isolates from different hosts and locations. Journal of Invertebrate Pathology 97, 9–13. doi: 10.1016/j.jip.2007.07.001.CrossRefGoogle ScholarPubMed
Hudson, R., Kreitman, M. and Aguade, M. (1987). A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153–159.CrossRefGoogle ScholarPubMed
Hudson, R., Boos, D. D. and Kaplan, N. L. (1992). A statistical test for detecting geographic subdivision. Molecular Biology and Evolution 9, 138–151.Google ScholarPubMed
Hudson, R. (2000). A new statistic for detecting genetic differentiation. Genetics 155, 2011–2014.CrossRefGoogle ScholarPubMed
Hudson, R. (2001). Two-locus sampling distributions and their application. Genetics 159, 1805–1817.CrossRefGoogle ScholarPubMed
Ironside, J. E. (2007). Multiple losses of sex within a single genus of Microsporidia. BMC Evolutionary Biology 7, 48. doi: 10.1186/1471-2148-7-48.CrossRefGoogle ScholarPubMed
Ironside, J. E. (2013). Diversity and recombination of dispersed ribosomal DNA and protein coding genes in microsporidia. PLoS ONE 8, e55878. doi: 10.1371/journal.pone.0055878.CrossRefGoogle ScholarPubMed
Jukes, T. H. and Cantor, C. R. (1969). Evolution of Protein Molecules. Academic Press, New York, USA.CrossRefGoogle Scholar
Klee, J., Besana, A. M., Genersch, E., Gisder, S., Nanetti, A., Tam, D. Q., Chinh, T. X., Puerta, F., Ruz, J. M., Kryger, P., Message, D., Hatjina, F., Korpela, S., Fries, I. and Paxton, R. J. (2007). Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera . Journal of Invertebrate Pathology 96, 1–10. doi: 10.1016/j.jip.2007.02.014.CrossRefGoogle ScholarPubMed
Lee, S. C., Corradi, N., Byrnes, E. J., Torres-Martinez, S., Dietrich, F. S., Keeling, P. J. and Heitman, J. (2008). Microsporidia evolved from ancestral sexual fungi. Current Biology 18, 1675–1679. doi: 10.1016/j.cub.2008.09.030.CrossRefGoogle ScholarPubMed
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452. doi: 10.1093/bioinformatics/btp187.CrossRefGoogle ScholarPubMed
Martín-Hernández, R., Meana, A., Prieto, L., Salvador, A. M., Garrido-Bailón, E. and Higes, M. (2007). Outcome of colonization of Apis mellifera by Nosema ceranae . Applied and Environmental Microbiology 73, 6331–6338. doi: 10.1128/AEM.00270-07.CrossRefGoogle ScholarPubMed
Martín-Hernández, R., Botías, C., Bailón, E. G., Martínez-Salvador, A., Prieto, L., Meana, A. and Higes, M. (2012). Microsporidia infecting Apis mellifera: coexistence or competition. Is Nosema ceranae replacing Nosema apis? Environmental Microbiology 14, 2127–2138. doi: 10.1111/j.1462-2920.2011.02645.x.CrossRefGoogle ScholarPubMed
McVean, G., Awadalla, P. and Fearnhead, P. (2002). A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160, 1231–1241.CrossRefGoogle ScholarPubMed
Myers, S. and Griffiths, R. C. (2003). Bounds on the minimum number of recombination events in a sample history. Genetics 163, 375–394.CrossRefGoogle Scholar
Nei, M. (1987). Molecular Evolutionary Genetics. Columbia University Press, New York, USA.CrossRefGoogle Scholar
O'Mahony, E. M., Tay, W. T. and Paxton, R. J. (2007). Multiple rRNA variants in a single spore of the microsporidian Nosema bombi . Journal of Eukaryotic Microbiology 54, 103–109. doi: 10.1111/j.1550-7408.2006.00232.x.CrossRefGoogle Scholar
Peyretaillade, E., Broussolle, V., Peyret, P., Metenier, G., Gouy, M. and Vivares, C. P. (1998). Microsporidia, amitochondrial protists, possess a 70-kDa heat shock protein gene of mitochondrial evolutionary origin. Molecular Biology and Evolution 15, 683–689. doi: 10.1093/oxfordjournals.molbev.a025971.CrossRefGoogle ScholarPubMed
Sagastume, S., Del Aguila, C., Martín-Hernández, R., Higes, M. and Henriques-Gil, N. (2011). Polymorphism and recombination for rDNA in the putatively asexual microsporidian Nosema ceranae, a pathogen of honeybees. Environmental Microbiology 13, 84–95. doi: 10.1111/j.1462-2920.2010.02311.x.CrossRefGoogle ScholarPubMed
Roudel, M., Aufauvre, J., Corbara, B., Delbac, F. and Blot, N. (2013). New insights on the genetic diversity of the honeybee parasite Nosema ceranae based on multilocus sequence analysis. Parasitology 140, 1346–1356.CrossRefGoogle ScholarPubMed
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Villa, J. D., Bourgeois, A. L. and Danka, R. G. (2013). Negative evidence for effects of genetic origin of bees on Nosema ceranae, positive evidence for effects of Nosema ceranae on bees. Apidologie 44, 511–518. doi: 10.1007/s13592-013-0201-1.CrossRefGoogle Scholar
Watterson, G. A. (1975). On the number of segregating sites in genetical models without recombination. Theoretical Population Biology 7, 256–276. doi: 10.1016/0040-5809(75)90020-9.CrossRefGoogle ScholarPubMed
Wittner, M. and Weiss, L. M. (1999). The Microsporidia and Microsporidosis, p. 110. ASM Press, Washington, DC, USA.CrossRefGoogle Scholar
Wright, S. and Charlesworth, B. (2004). The HKA test revisited a maximum-likelihood-ratio test of the standard neutral model. Genetics 168, 1071–1076. doi: 10.1534/genetics.104.026500 Note.CrossRefGoogle ScholarPubMed
Yang, Z. (2007). PAML 4: a program package for phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24, 1586–1591.CrossRefGoogle ScholarPubMed
Yang, Z. and Nielsen, R. (2000). Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Molecular Biology and Evolution 17, 32–43.CrossRefGoogle ScholarPubMed
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