Detection and quantification of Melissococcus plutonius in honey bee workers exposed to European foulbrood in Czechia through conventional PCR, qPCR, and barcode sequencing

References

• Anderson, M. J., Ellingsen, K. E., & McArdle, B. H. (2006). Multivariate dispersion as a measure of beta diversity. Ecology Letters, 9(6), 683–693. doi:10.1111/j.1461-0248.2006.00926.x
   PubMed Web of Science ®Google Scholar
• Bailey, L. (1961). European foulbrood. American Bee Journal, 101, 89–92.
   Google Scholar
• Bailey, L. (1963). The pathogenicity for honey-bee larvae of microorganisms associated with European foulbrood. Journal of Insect Pathology, 5(2), 198–205.
   Google Scholar
• Belloy, L., Imdorf, A., Fries, I., Forsgren, E., Berthoud, H., Kuhn, R., & Charriere, J.-D. (2007). Spatial distribution of Melissococcus plutonius in adult honey bees collected from apiaries and colonies with and without symptoms of European foulbrood. Apidologie, 38(2), 136–140. doi:10.1051/apido:2006069
   Web of Science ®Google Scholar
• Budge, G. E., Barrett, B., Jones, B., Pietravalle, S., Marris, G., Chantawannakul, P., … Brown, M. A. (2010). The occurrence of Melissococcus plutonius in healthy colonies of Apis mellifera and the efficacy of European foulbrood control measures. Journal of Invertebrate Pathology, 105(2), 164–170. doi:10.1016/j.jip.2010.06.004
   PubMed Web of Science ®Google Scholar
• Caporaso, J. G., Lauber, C. L., Walters, W. A., Berg-Lyons, D., Huntley, J., Fierer, N., … Knight, R. (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME Journal, 6(8), 1621–1624. doi:10.1038/ismej.2012.8
   PubMed Web of Science ®Google Scholar
• Chen, Y. P., Higgins, J. A., & Feldlaufer, M. F. (2005). Quantitative real-time reverse transcription-PCR analysis of deformed wing virus infection in the honeybee (Apis mellifera L.). Applied and Environmental Microbiology, 71(1), 436–441. doi:10.1128/AEM.71.1.436-441.2005
   PubMed Web of Science ®Google Scholar
• Cole, J. R., Wang, Q., Fish, J. A., Chai, B., McGarrell, D. M., Sun, Y., … Tiedje, J. M. (2014). Ribosomal database project: Data and tools for high throughput rRNA analysis. Nucleic Acids Research, 42(D1), D633–D642. doi:10.1093/nar/gkt1244
   PubMed Web of Science ®Google Scholar
• Dainat, B., Grossar, D., Ecoffey, B., & Haldemann, C. (2018). Triplex real-time PCR method for the qualitative detection of European and American foulbrood in honeybee. Journal of Microbiological Methods, 146, 61–63. doi:10.1016/j.mimet.2018.01.018
   PubMed Web of Science ®Google Scholar
• Dorn‐In, S., Bassitta, R., Schwaiger, K., Bauer, J., & Holzel, C. S. (2015). Specific amplification of bacterial DNA by optimized so-called universal bacterial primers in samples rich of plant DNA. Journal of Microbiological Methods, 113, 50–56. doi:10.1016/j.mimet.2015.04.001
   PubMed Web of Science ®Google Scholar
• Earley, Z. M., Akhtar, S., Green, S. J., Naqib, A., Khan, O., Cannon, A. R., … Choudhry, M. A. (2015). Burn injury alters the intestinal microbiome and increases gut permeability and bacterial translocation. PLoS One, 10(7), e0129996. doi:10.1371/journal.pone.0129996
   PubMed Web of Science ®Google Scholar
• Edgar, R. C. (2013). UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10), 996–998. doi:10.1038/nmeth.2604
   PubMed Web of Science ®Google Scholar
• Edgar, R. C. (2016). UNOISE2: Improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv. doi:10.1101/081257
   Google Scholar
• Erban, T., Ledvinka, O., Kamler, M., Hortova, B., Nesvorna, M., Tyl, J., … Hubert, J. (2017). Bacterial community associated with worker honeybees (Apis mellifera) affected by European foulbrood. PeerJ, 5, e3816. doi:10.7717/peerj.3816
   PubMed Web of Science ®Google Scholar
• Erler, S., Lewkowski, O., Poehlein, A., & Forsgren, E. (2018). The curious case of Achromobacter eurydice, a Gram-variable pleomorphic bacterium associated with European foulbrood disease in honeybees. Microbial Ecology, 75(1), 1–6. doi:10.1007/s00248-017-1007-x
   PubMed Web of Science ®Google Scholar
• Forsgren, E. (2010). European foulbrood in honey bees. Journal of Invertebrate Pathology, 103(Suppl. 1), S5–S9. doi:10.1016/j.jip.2009.06.016
   PubMed Web of Science ®Google Scholar
• Forsgren, E., Budge, G. E., Charriere, J.-D., & Hornitzky, M. A. Z. (2013). Standard methods for European foulbrood research. Journal of Apicultural Research, 52(1), 1. 52.1.12. doi:10.3896/IBRA.1.52.1.12
   Web of Science ®Google Scholar
• Forsgren, E., Locke, B., Sircoulomb, F., & Schafer, M. O. (2018). Bacterial diseases in honeybees. Current Clinical Microbiology Reports, 5(1), 18–25. doi:10.1007/s40588-018-0083-0
   Web of Science ®Google Scholar
• Forsgren, E., Lundhagen, A. C., Imdorf, A., & Fries, I. (2005). Distribution of Melissococcus plutonius in honeybee colonies with and without symptoms of European foulbrood. Microbial Ecology, 50(3), 369–374. doi:10.1007/s00248-004-0188-2
   PubMed Web of Science ®Google Scholar
• Gaggia, F., Baffoni, L., Stenico, V., Alberoni, D., Buglione, E., Lilli, A., … Porrini, C. (2015). Microbial investigation on honey bee larvae showing atypical symptoms of European foulbrood. Bulletin of Insectology, 68(2), 321–327.
   Web of Science ®Google Scholar
• Garrido-Bailon, E., Higes, M., Martinez-Salvador, A., Antunez, K., Botias, C., Meana, A., … Martin-Hernandez, R. (2013). The prevalence of the honeybee brood pathogens Ascosphaera apis, Paenibacillus larvae and Melissococcus plutonius in Spanish apiaries determined with a new multiplex PCR assay. Microbial Biotechnology, 6(6), 731–739. doi:10.1111/1751-7915.12070
   PubMed Web of Science ®Google Scholar
• Govan, V. A., Brozel, V., Allsopp, M. H., & Davison, S. (1998). A PCR detection method for rapid identification of Melissococcus pluton in honeybee larvae. Applied and Environmental Microbiology, 64(5), 1983–1985.
   PubMed Web of Science ®Google Scholar
• Grangier, V., Belloy, L., Charriere, J.-D., Doherr, M. G., Fritsche, A., & Waldvogel, A. S. (2015). Real-time PCR as a decision aid in the control of European foulbrood. Journal of Apicultural Research, 54(4), 366–372. doi:10.1080/00218839.2016.1169650
   Web of Science ®Google Scholar
• Hammer, O., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 4. Retrieved from http://palaeo-electronica.org/2001_1/past/issue1_01.htm
   Google Scholar
• Hubert, J., Bicianova, M., Ledvinka, O., Kamler, M., Lester, P. J., Nesvorna, M., … Erban, T. (2017). Changes in the bacteriome of honey bees associated with the parasite Varroa destructor, and pathogens Nosema and Lotmaria passim. Microbial Ecology, 73(3), 685–698. doi:10.1007/s00248-016-0869-7
   PubMed Web of Science ®Google Scholar
• Hubert, J., Erban, T., Kamler, M., Kopecky, J., Nesvorna, M., Hejdankova, S., … Zurek, L. (2015). Bacteria detected in the honeybee parasitic mite Varroa destructor collected from beehive winter debris. Journal of Applied Microbiology, 119(3), 640–654. doi:10.1111/jam.12899
   PubMed Web of Science ®Google Scholar
• Kesnerova, L., Moritz, R., & Engel, P. (2016). Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria. International Journal of Systematic and Evolutionary Microbiology, 66(1), 414–421. doi:10.1099/ijsem.0.000736
   PubMed Web of Science ®Google Scholar
• Killer, J., Dubna, S., Sedlacek, I., & Svec, P. (2014). Lactobacillus apis sp. nov., from the stomach of honeybees (Apis mellifera), having an in vitro inhibitory effect on the causative agents of American and European foulbrood. International Journal of Systematic and Evolutionary Microbiology, 64(Pt 1), 152–157. doi:10.1099/ijs.0.053033-0
   PubMed Web of Science ®Google Scholar
• Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., & Schloss, P. D. (2013). Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Applied and Environmental Microbiology, 79(17), 5112–5120. doi:10.1128/AEM.01043-13
   PubMed Web of Science ®Google Scholar
• Kwong, W. K., & Moran, N. A. (2016). Apibacter adventoris gen. nov., sp. nov., a member of the phylum Bacteroidetes isolated from honey bees. International Journal of Systematic and Evolutionary Microbiology, 66(3), 1323–1329. doi:10.1099/ijsem.0.000882
   PubMed Web of Science ®Google Scholar
• Kwong, W. K., Steele, M. I., & Moran, N. A. (2018). Genome sequences of Apibacter spp., gut symbionts of Asian honey bees. Genome Biology and Evolution, 10(4), 1174–1179. doi:10.1093/gbe/evy076
   PubMed Web of Science ®Google Scholar
• Lane, D. J. (1991). 16s/23s rRNA sequencing. In E. Stackebrandt & M. Goodfellow (Eds.), Nucleic acid techniques in bacterial systematics (pp. 115–175). Chichester, UK: John Wiley and Sons.
   Google Scholar
• Legendre, P., & Gallagher, E. D. (2001). Ecologically meaningful transformations for ordination of species data. Oecologia, 129(2), 271–280. doi:10.1007/s004420100716
   PubMed Web of Science ®Google Scholar
• Lewkowski, O., & Erler, S. (2019). Virulence of Melissococcus plutonius and secondary invaders associated with European foulbrood disease of the honey bee. MicrobiologyOpen, 8(3), e00649. doi:10.1002/mbo3.649
   PubMed Web of Science ®Google Scholar
• MA. (2018). Vyhlaska c. 18/2018 ze dne 31. ledna 2018 o veterinarnich pozadavcich na chov vcel a vcelstev a o opatrenich pro predchazeni a zdolavani nekterých nakaz vcel a o zmene nekterych souvisejicich vyhlasek [Decree No 18/2018 Coll. from 31st January 2018 about veterinary requirements for beekeeping, and measures to prevent and combat certain diseases and amending certain related decrees]. In Collection of laws of the Czech Republic, part 12/2018, 7th February 2018 (pp. 253–259). Prague: Ministry of Agriculture of the Czech Republic (MA CR). Retrieved from http://eagri.cz/public/web/mze/ministerstvo-zemedelstvi/legislativa/prijate-predpisy-mze-dosud-neucinne/vyhlaska-c-18-2018-sb.html (in Czech)
   Google Scholar
• McKee, B. A., Djordjevic, S. P., Goodman, R. D., & Hornitzky, M. A. (2003). The detection of Melissococcus pluton in honey bees (Apis mellifera) and their products using a hemi-nested PCR. Apidologie, 34(1), 19–27. doi:10.1051/apido:2002047
   Web of Science ®Google Scholar
• McNemar, Q. (1947). Note on the sampling error of the difference between correlated proportions or percentages. Psychometrika, 12(2), 153–157. doi:10.1007/bf02295996
   Google Scholar
• Mockler, B. K., Kwong, W. K., Moran, N. A., & Koch, H. (2018). Microbiome structure influences infection by the parasite Crithidia bombi in bumble bees. Applied and Environmental Microbiology, 84(7), e02335–17. doi:10.1128/AEM.02335-17
   PubMed Web of Science ®Google Scholar
• Motta, E. V. S., Raymann, K., & Moran, N. A. (2018). Glyphosate perturbs the gut microbiota of honey bees. Proceedings of the National Academy of Sciences of the United States of America, 115(41), 10305–10310. doi:10.1073/pnas.1803880115
   PubMed Web of Science ®Google Scholar
• Nakamura, K., Yamazaki, Y., Shiraishi, A., Kobayashi, S., Harada, M., Yoshiyama, M., … Takamatsu, D. (2016). Virulence differences among Melissococcus plutonius strains with different genetic backgrounds in Apis mellifera larvae under an improved experimental condition. Scientific Reports, 6(1), 33329. doi:10.1038/srep33329
   PubMed Web of Science ®Google Scholar
• OIE. (2018). Diseases of bees. Paris: World Organisation for Animal Health (OIE). Retrieved from http://www.oie.int/en/animal-health-in-the-world/animal-diseases/diseases-of-bees/
   Google Scholar
• Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., … Wagner, H. (2016). vegan: Community ecology package. CRAN - The Comprehensive R Archive Network. Retrieved from http://CRAN.R-project.org/package=vegan
   Google Scholar
• Ondov, B. D., Bergman, N. H., & Phillippy, A. M. (2011). Interactive metagenomic visualization in a web browser. BMC Bioinformatics, 12(1), 385. doi:10.1186/1471-2105-12-385
   PubMed Web of Science ®Google Scholar
• Pinnock, D. E., & Featherstone, N. E. (1984). Detection and quantification of Melissococcus pluton infection in honeybee colonies by means of enzyme-linked immunosorbent assay. Journal of Apicultural Research, 23(3), 168–170. doi:10.1080/00218839.1984.11100627
   Web of Science ®Google Scholar
• Powell, J. E., Martinson, V. G., Urban-Mead, K., & Moran, N. A. (2014). Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Applied and Environmental Microbiology, 80(23), 7378–7387. doi:10.1128/AEM.01861-14
   PubMed Web of Science ®Google Scholar
• Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., … Glöckner, F. O. (2012). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(D1), D590–D596. doi:10.1093/nar/gks1219
   PubMed Web of Science ®Google Scholar
• R Core Team. (2018). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Retrieved from http://www.R-project.org
   Google Scholar
• Raymann, K., & Moran, N. A. (2018). The role of the gut microbiome in health and disease of adult honey bee workers. Current Opinion in Insect Science, 26, 97–104. doi:10.1016/j.cois.2018.02.012
   PubMed Web of Science ®Google Scholar
• Roetschi, A., Berthoud, H., Kuhn, R., & Imdorf, A. (2008). Infection rate based on quantitative real-time PCR of Melissococcus plutonius, the causal agent of European foulbrood, in honeybee colonies before and after apiary sanitation. Apidologie, 39(3), 362–371. doi:10.1051/apido:200819
   Web of Science ®Google Scholar
• Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., … Weber, C. F. (2009). Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75(23), 7537–7541. doi:10.1128/AEM.01541-09
   PubMed Web of Science ®Google Scholar
• Segers, F. H. I. D., Kesnerova, L., Kosoy, M., & Engel, P. (2017). Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen. ISME Journal, 11(5), 1232–1244. doi:10.1038/ismej.2016.201
   PubMed Web of Science ®Google Scholar
• Sing, T., Sander, O., Beerenwinkel, N., & Lengauer, T. (2005). ROCR: Visualizing classifier performance in R. Bioinformatics, 21(20), 3940–3941. doi:10.1093/bioinformatics/bti623
   Google Scholar
• Stock, C., & Hielscher, T. (2014). DTComPair: Comparison of binary diagnostic tests in a paired study design, R package version 1.0.3. CRAN - The Comprehensive R Archive Network. Retrieved from http://CRAN.R-project.org/package=DTComPair
   Google Scholar
• Takamatsu, D., Sato, M., & Yoshiyama, M. (2016). Infection of Melissococcus plutonius clonal complex 12 strain in European honeybee larvae is essentially confined to the digestive tract. Journal of Veterinary Medical Science, 78(1), 29–34. doi:10.1292/jvms.15-0405
   PubMed Web of Science ®Google Scholar
• Vasquez, A., Forsgren, E., Fries, I., Paxton, R. J., Flaberg, E., Szekely, L., & Olofsson, T. C. (2012). Symbionts as major modulators of insect health: Lactic acid bacteria and honeybees. PLoS One, 7(3), e33188. doi:10.1371/journal.pone.0033188
   PubMed Web of Science ®Google Scholar
• Waite, R. J., Brown, M. A., Thompson, H. M., & Bew, M. H. (2003). Controlling European foulbrood with the shook swarm method and oxytetracycline in the UK. Apidologie, 34(6), 569–575. doi:10.1051/apido:2003052
   Web of Science ®Google Scholar
• White, J. R., Nagarajan, N., & Pop, M. (2009). Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Computational Biology, 5(4), e1000352. doi:10.1371/journal.pcbi.1000352
   PubMed Web of Science ®Google Scholar
• Zeleny, D. (2018). Analysis of community ecology data in R. DavidZeleny.net. Retrieved from https://www.davidzeleny.net/anadat-r/doku.php/en
   Google Scholar