Effects of Bacterial Cell-Free Supernatant on Nutritional Parameters of Apis Mellifera and Their Toxicity Against Varroa Destructor
References
- 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 - 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 - 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 - 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 - 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 - 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 . - 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 - 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 - 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 - 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 - 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 - 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 - 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.
- 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 - 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 - 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 - 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 - 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 - 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 - 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.
- 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.
- 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 - 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 . - 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 - 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 - 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 - 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 - 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 - 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 . - 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 - 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 . - 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 - 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 - 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 - 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 - 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 - 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 - 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 - 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 . - 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.
- 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 - 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 - 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 - 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/S1431927618006773RamseyS.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
- 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.
- 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 - 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 - 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 - 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 - 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 - 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 - Tewarson, N. C. (1983). Nutrition and reproduction in the ectoparasitic honey bee (Apis sp.) mite, Varroa jacobsoni. Eberhard-Karls-Universität Tübingen.
- 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 - 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 - 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 - 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
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
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© 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
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