Have a personal or library account? Click to login

Effects of Bacterial Cell-Free Supernatant on Nutritional Parameters of Apis Mellifera and Their Toxicity Against Varroa Destructor

Open Access
|Jul 2020

References

  1. Alberoni, D., Gaggìa, F., Baffoni, L., & Di Gioia, D. (2016). Beneficial microorganisms for honey bees: problems and progresses. Applied Microbiology and Biotechnology, 100, 9469–9482. https://doi.org/10.1007/s00253-016-7870-4
  2. Ament, S. A., Chan, Q. W., Wheeler, M. M., Nixon, S. E., Johnson, S. P.,... Robinson, G. E. (2011). Mechanisms of stable lipid loss in a social insect. Journal of Experimental Biology, 214(22), 3808–3821. https://doi.org/10.1242/jeb.060244
  3. Amdam, G. V., Hartfelder, K., Norberg, K., Hagen, A., Omholt, S. W. (2004). Altered Physiology in Worker Honey Bees (Hymenoptera: Apidae) Infested with the Mite Varroa destructor (Acari: Varroidae): A Factor in Colony Loss During Overwintering? Journal of Economic Entomology, 97(3), 741–747. https://doi.org/10.1093/jee/97.3.741
  4. Antúnez, K., Anido, M., Branchiccela, B., Harriet, J., Campa, J., ... Zunino, P. (2015). Seasonal variation of honeybee pathogens and its association with pollen diversity in Uruguay. Microbial ecology, 70(2), 522–533. https://doi.org/10.1007/s00248-015-0594-7
  5. Arrese, E. L., & Soulages, J. L. (2010). Insect fat body: energy, metabolism, and regulation. Annual review of entomology, 55, 207–225. https://doi.org/10.1146/annurev-ento-112408-085356
  6. Audisio, M. A. (2016). Gram-Positive Bacteria with Probiotic Potential for the Apis mellifera L. Honey Bee: The Experience in the Northwest of Argentina. Probiotics and Antimicrobial Proteins. https://doi.org/10.1007/s12602-016-9231-0.
  7. Audisio, M. C., & Benítez-Ahrendts, M. R. (2011). Lactobacillus johnsonii CRL1647, isolated from Apis mellifera L. bee-gut, exhibited a beneficial effect on honeybee colonies. Beneficial Microbes, 2(1), 29–34. https://doi.org/10.3920/BM2010.0024
  8. Audisio, M. C., Terzolo, H. R., & Apella, M. C. (2005). Bacteriocin from honeybee beebread Enterococcus avium, active against Listeria monocytogenes. Applied and Environmental Microbiology, 71(6), 3373–3375. https://doi.org/10.1128/AEM.71.6.3373-3375.2005
  9. Audisio, M. C., Sabaté, D. C., & Benítez-Ahrendts, M. R. (2015). Effect of Lactobacillus johnsonii CRL1647 on different parameters of honeybee colonies and bacterial populations of the bee gut. Beneficial Microbes, 25, 1–10. https://doi.org/10.3920/BM2014.0155
  10. Baffoni, L., Gaggìa, F., Alberoni, D., Cabbri, R., Nanetti, A., … Di Gioia, D. (2016). Effect of dietary supplementation of Bifidobacterium and Lactobacillus strains in Apis mellifera L. against Nosema ceranae. Beneficial microbes, 7(1), 45–51. https://doi.org/10.3920/BM2015.0085
  11. Bahreini, R., & Currie, R. W. (2015). The influence of Nosema (Microspora: Nosematidae) infection on honey bee (Hymenoptera: Apidae) defense against Varroa destructor (Mesostigmata: Varroidae). Journal of Invertebrate Pathology, 132, 57–65. https://doi.org/10.1016/j.jip.2015.07.019
  12. Bowen-Walker, P. L., & Gunn, A. (2001). The effect of the ectoparasitic mite, Varroa destructor on adult worker honeybee (Apis mellifera) emergence weights, water, protein, carbohydrate, and lipid levels. Entomologia Experimentails et Applicata, 101(3), 207–217. https://doi.org/10.1046/j.1570-7458.2001.00905.x
  13. Bradford, M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye-binding. Analytical Biochemistry, 72, 248–254.
  14. Brodschneider, R. & Crailsheim, K. (2010). Nutrition and health in honey bees. Apidologie, 41(3), 278–294. https://doi.org/10.1016/0003-2697(76)90527-3
  15. Caccia, S., Di Lelio, I., La Storia, A., Marinelli, A., Varricchio, P., ... Ferré, J. (2016). Midgut microbiota and host immunocompetence underlie Bacillus thuringiensis killing mechanism. Proceedings of the National Academy of Sciences, 113(34), 9486–9491. https://doi.org/10.1073/pnas.1521741113
  16. Corona, M., Velarde, R. A., Remolina, S., Moran-Lauter, A., Wang, Y., … Robinson, G. E. (2007). Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. Proceedings of the National Academy of Sciences, 104(17), 7128–7133. https://doi.org/10.1073/pnas.0701909104
  17. Crotti, E., Balloi, A., Hamdi, C., Sansonno, L., Marzorati, M. (2012). Microbial symbionts: a resource for the management of insect-related problems. Microbial Biotechnology, 5, 307–317. https://doi.org/10.1111/j.1751-7915.2011.00312.x
  18. Crotti, E., Sansonno, L., Prosdocimi, E. M., Vacchini, V., Hamdi, C.,... Balloi, A. (2013). Microbial symbionts of honeybees: a promising tool to improve honeybee health. New biotechnology, 30(6), 716–722. https://doi.org/10.1016/j.nbt.2013.05.004
  19. Damiani, N., Maggi, M. D., Gende, L. B., Faverin, C., Eguaras, M. J., Marcangeli, J. A. (2010). Evaluation of the toxicity of a propolis extract on Varroa destructor (Acari: Varroidae) and Apis mellifera (Hymenoptera: Apidae). Journal of Apicultural Research, 49(3), 257–264. https://doi.org/10.3896/IBRA.1.49.3.05
  20. De D’Aubeterre, J. P., Myrold, D.D., Royce, L. A., & Rossignol, P. A. (1999). A scientific note of an application of isotope ratio mass spectrometry to feeding by the mite, Varroa jacobsoni Oudemans, on the honeybee, Apis mellifera L. Apidologie 30, 351–352.
  21. De Oliveira, V. T. P., & Da Cruz-Landim, C. (2003). Morphology and function of insect fat body cells: a review. Biociências, 11 (2), 195–205.
  22. Engel, P., Martinson, V. G., & Moran, N. A. (2012). Functional diversity within the simple gut microbiota of the honey bee. Proceedings of the National Academy of Sciences, 109(27), 11002–11007. https://doi.org/10.1073/pnas.1202970109
  23. European Commission, (2010). Commission Regulation (EU) No 37/2010 of 22 December 2009 on pharmacologically active substances and their classification regarding maximum residue limits in foodstuffs of animal origin. Official Journal of the European Union, 15, 1–70. http://ec.europa.eu/health/files/eudralex/vol-5/reg_2010_37/reg_2010_37_en.pdf.
  24. Gregory, P. G., Evans, J. D., Rinderer, T., & De Guzman, L. (2005). Conditional immune-gene suppression of honeybees parasitized by Varroa mites. Journal of Insect Science, 5, 7. https://doi.org/10.1093/jis/5.1.7
  25. Hubert, J., Bicianova, M., Ledvinka, O., Kamler, M., Lester, P. J.,... 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. https://doi.org/10.1007/s00248-016-0869-7
  26. Janashia, I. & Alaux, C. (2016). Specific Immune Stimulation by Endogenous Bacteria in Honey Bees (Hymenoptera: Apidae). Journal of Economic Entomology, https://doi.org/10.1093/jee/tow065
  27. Jefferson, J. M., Dolstad, H. A., Sivalingam, M. D., & Snow, J. W. (2013). Barrier immune effectors are maintained during transition from nurse to forager in the honey bee. PLoS ONE, https://doi.org/10.1371/journal.pone.0054097
  28. Kakumanu, M. L., Reeves, M. R., Anderson, T. D., Rodrigues, R. R., Williams, M. A. (2016). Honey Bee Gut Microbiome Is Altered by In-Hive Pesticide Exposures. Frontiers in Microbiology, 7, 1255. https://doi.org/10.3389/fmicb.2016.01255
  29. Kesïnerova, Â. L., Mars, R. A. T., Ellegaard, K. M., Troilo, M., Sauer, U., Engel, P. (2017). Disentangling metabolic functions of bacteria in the honey bee gut. PLoS Biol, 15(12): e2003467. https://doi.org/10.1371/journal.pbio.2003467.
  30. Kwong, W. K., & Moran, N. A. (2016). Gut microbial communities of social bees. Nature Reviews Microbiology, 14, 374–384. https://doi.org/10.1038/nrmicro.2016.43
  31. Kwong, W. K., Mancenido, A. L., & Moran, N. A. (2017). Immune system stimulation by the native gut microbiota of honey bees. Royal Society open Science, 4, 170003. http://dx.doi.org/10.1098/rsos.170003.
  32. Lee, K. V., Steinhauer, N., Rennich, K., Wilson, M. E., Tarpy, D. R., ... Pettis, J. (2015). A national survey of managed honey bee 2013–2014 annual colony losses in the USA. Apidologie, 46(3), 292–305. https://doi.org/10.1007/s13592-015-0356-z
  33. Maggi, M., Negri, P., Plischuk, S., Szawarski, N., De Piano, F.,... Audisio, C. (2013). Effects of the organic acids produced by a lactic acid bacterium in Apis mellifera colony development, Nosema ceranae control and fumagillin efficiency. Veterinary Microbiology, 167(3–4), 474–483. https://doi.org/10.1016/j.vetmic.2013.07.030
  34. Maggi, M., Antúnez, K., Invernizzi, C., Aldea, P., Vargas, M., ... Barrios, C. (2016). Honeybee health in South America. Apidologie, 47(6), 835–854. https://doi.org/10.1007/s13592-016-0445-7
  35. Márquez Gutiérrez, M. E., Fernández-Larrea, Vega, O., Díaz Mena, D., Díaz, A., Carreras Solís, B. (2003). Evaluación de un producto de Bacillus thuringiensis para el control de la varroasis. Fitosanidad, 7, 1. http://www.redalyc.org/articulo.oa?id=209118077001
  36. Medici, S. K., Maggi, M. D., Sarlo, E. G., Ruffinengo, S., … Eguaras, M. J. (2015). The presence of synthetic acaricides in beeswax and its influence on the development of resistance in Varroa destructor. Journal of Apicultural Research, 54(3), 267–274. https://doi.org/10.1080/00218839.2016.1145407
  37. Moran, N. A. (2015). Genomics of the honey bee microbiome. Current Opinion Insect Science, 10, 22–28. https://doi.org/10.1016/j.cois.2015.04.003
  38. Neumann, P., & Carreck, N. L. (2010). Honey bee colony losses. Journal of Apicultural Research, 49(1), 1–6. https://doi.org/10.3896/IBRA.1.49.1.01
  39. Newton, I. L., Sheehan, K. B., Lee, F.J., Horton, M. A., Hicks, R. D. (2013). Invertebrate systems for hypothesis-driven microbiome research. Microbiome Science and Medicine, 1(1). https://doi.org/10.2478/micsm-2013-0001.
  40. Nieto, A., Roberts, S. P., Kemp, J., Rasmont, P., Kuhlmann, M., ... De Meulemeester, T. (2014). European red list of bees. Luxembourg: Publication Office of the European Union, 98. Luxembourgo.
  41. Nilsen, K. A., Ihle, K. E., Frederick, K., Fondrk, M. K., Smedal, B. (2010). Insulin-like peptide genes in honey bee fat body respond differently to manipulation of social behavioral physiology. Journal of Experimental Biology, 214, 1488–1497. https://doi.org/10.1242/jeb.050393
  42. Ptaszyńska, A. A., Borsuk, G., Zdybicka-Barabas, A., Cytryńska, M., Małek, W. (2016). Arecommercial probiotics and prebiotics effective in the treatment and prevention of honeybee nosemosis C? Parasitology Research, 115, 397–406. https://doi.org/10.1007/s00436-015-4761-z
  43. Porrini, M. P., Audisio, M. C., Sabaté, D. C., Ibarguren, C., Medici, S. K.,... Eguaras, M. J. (2010). Effect of bacterial metabolites on microsporidian Nosema ceranae and on its host Apis mellifera. Parasitology research, 107(2), 381–388. https://doi.org/10.1007/s00436-010-1875-1
  44. Ramsey, S., Gulbronson, C. J., Mowery, J., Ochoa, R., Bauchan, G. (2018). A multi-microscopy approach to discover the feeding site and host tissue consumed by Varroa destructor on host honey bees. Microscopy and Microanalysis, 24(S1), 1258–1259. DOI: 10.1017/S1431927618006773
    RamseyS.GulbronsonC. J.MoweryJ.OchoaR.BauchanG.2018A multi-microscopy approach to discover the feeding site and host tissue consumed by Varroa destructor on host honey beesMicroscopy and Microanalysis24S11258125910.1017/S1431927618006773
  45. Ramsey, S. D., Ochoa, R., Bauchan, G., Gulbronson, C., Mowery, J. D., Cohen, A., ... Hawthorne, D. (2019). Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proceedings of the National Academy of Sciences, 116(5), 1792–1801.
  46. Ruffinengo, S., Eguaras, M., Floris, I., Faverin, C., Bailac, P., Ponzi, M. (2005). LD50 and repellent effect to Varroa destructor mite of different essential oil from Argentina wild plants species. Journal of Economic Entomology, 98(3), 651–655. https://doi.org/10.1603/0022-0493-98.3.651
  47. Sabaté, D. C., Carrillo, L., & Audisio, M. C. (2009). Inhibition of Paenibacillus larvae and Ascosphaera apis by Bacillus subtilis isolated from honeybee gut and honey samples. Research Microbiology, 160, 193–199. https://doi.org/10.1016/j.resmic.2009.03.002
  48. Sabaté, D. C., Cruz, M. S., Benítez-Ahrendts, M. R., Audisio, M. C. (2012). Beneficial Effects of Bacillus subtilis subsp. subtilis Mori2, a Honey-Associated Strain, on Honeybee Colony Performance. Probiotics and Antimicrobial Proteins, 4, 39–46. https://doi.org/10.1007/s12602-011-9089-0
  49. Sandionigi, A., Vicario, S., Prosdocimi, E. M., Galimberti, A., Ferri, E., Bruno, A., ... Casiraghi, M. (2015). Towards a better understanding of Apis mellifera and Varroa destructor microbiomes: introducing ‘phyloh’as a novel phylogenetic diversity analysis tool. Molecular ecology resources, 15(4), 697–710. https://doi.org/10.1111/1755-0998.12341
  50. Seitz, N., Traynor, K. S., Steinhauer, N., Rennich, K., Wilson, M. E.,... Delaplane, K. S. (2015). A national survey of managed honey bee 2014–2015 annual colony losses in the USA. Journal of Apicultural Research, 54(4), 292–304. https://doi.org/10.1080/00218839.2016.1153294
  51. Simion, G., Trif, A., Cara, M. C., & Damiescu, L. (2011). Evaluation of tetracyclines’ and cloramphenicol's residues levels in honey from Timis County between 2007 and 2010. Lucrari Stiintifice-Universitatea de Stiinte Agricole a Banatului Timisoara. Medicina Veterinaria, 41(1): 264–269. https://www.cabdirect.org/cabdirect/abstract/20113378205
  52. Tewarson, N. C. (1983). Nutrition and reproduction in the ectoparasitic honey bee (Apis sp.) mite, Varroa jacobsoni. Eberhard-Karls-Universität Tübingen.
  53. Torres, M. J., Petroselli, G., Daz, M., Erra-Balsells, R., Audisio, M. C. (2015). Bacillus subtilis subsp. subtilis CBMDC3f with antimicrobial activity against Gram-positive foodborne pathogenic bacteria. UV-MALDI-TOF MS analysis of its bioactive compounds. World Journal of Microbiology and Biotechnology, 31(6), 929–940. https://doi.org/10.1007/s11274-015-1847-9
  54. Vásquez, A., Forsgren, E., Fries, I., Paxton, R., Flaberg, E. (2012). Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS ONE. https://doi.org/10.1371/journal.pone.0033188
  55. Watson, K., & Stallins, A. (2016). Honey Bees and Colony Collapse Disorder: A Pluralistic Reframing. Geography Compass, 10(5), 222–236. https://doi.org/10.1111/gec3.12266
  56. Wilson-Rich, N., Dres, S. T., & Starks, P. T. (2008). The ontogeny of immunity: development of innate immune strength in the honey bee (Apis mellifera). Journal of Insect Physiology, 54(10–11), 1392–1399. https://doi.org/10.1016/j.jinsphys.2008.07.016
DOI: https://doi.org/10.2478/jas-2020-0009 | Journal eISSN: 2299-4831 | Journal ISSN: 1643-4439
Language: English
Page range: 55 - 66
Submitted on: Apr 4, 2019
Accepted on: Feb 11, 2020
Published on: Jul 2, 2020
Published by: Research Institute of Horticulture
In partnership with: Paradigm Publishing Services
Publication frequency: 2 issues per year

© 2020 Fiorella G. De Piano, Matias D. Maggi, Facundo R. Meroi Arceitto, Marcela C. Audisio, Martín Eguaras, Sergio R. Ruffinengo, published by Research Institute of Horticulture
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.