The dose makes the poison: feeding of antibiotic-treated winter honey bees, Apis mellifera, with probiotics and b-vitamins
Tóm tắt
Honey stores of Apis mellifera colonies are replaced with sugar water by beekeepers, which may result in malnutrition. Nutritional supplements have been developed, but the importance of bacterial probiotics and vitamins is poorly understood. Given that supplementary feeding with vitamins and probiotics may enhance worker weight and longevity, this might suggest a feasible approach to mitigate winter colony losses. Here, we conducted a laboratory hoarding cage study with freshly emerged winter bees, which were treated with the antibiotic tetracycline to reduce gut bacteria obtained post-emergence and subsequently assigned to feeding regimes: sucrose only, sucrose + pollen, probiotics (low and high dosage), probiotics + pollen (low and high dosage), or b-vitamins (low and high dosage) (N = 8 treatments, 29 workers/cage × 8 replicates). In parallel, another age cohort of bees remained on their frame (= Frame) to establish their gut microbiota and were subsequently fed with sucrose only or sucrose + pollen (N = 2 treatments, 29 workers/cage × 4 replicates). The most beneficial effects on body weights were found in workers given ad libitum access to pollen, notably in the Frame Sucrose + Pollen group, confirming the inherent importance of post-emergent gut flora inoculation and the role of gut bacteria in protein digestion. Furthermore, both Frame groups and the antibiotic-treated workers fed with probiotic low + pollen survived longer than all other groups, highlighting a fundamental host-microbial relationship. On the other hand, our current treatments alone, post-tetracycline, did not yield any positive results. In contrast, high dosages of both probiotic and b-vitamins significantly reduced lifespan compared to their low concentration counterparts, probably due to dysbiosis and toxicity, suggesting that the outcome was dose-dependent. These results highlight that bacterial and b-vitamin supplementation can alter longevity with advisable caution since harmful concentrations appear to exist.
Tài liệu tham khảo
Altaye, S. Z., Pirk, C. W. W., Crewe, R. M., & Nicolson, S. W. (2010). Convergence of carbohydrate-biased intake targets in caged worker honeybees fed different protein sources. Journal of Experimental Biology, 213(19). https://doi.org/10.1242/jeb.046953
Anderson, L. M., & Dietz, A. (1976). Pyridoxine requirement of the honey bee (Apis mellifera) for brood rearing. Apidologie, 7(1). https://doi.org/10.1051/apido:19760105
Bäckhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A., & Gordon, J. I. (2005). Host-bacterial mutualism in the human intestine. Science, 307(5717). https://doi.org/10.1126/science.1104816
Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software, 67(1), 1-48. https://doi.org/10.18637/jss.v067.i01
Bogdanov, S., Jurendic, T., Sieber, R., & Gallmann, P. (2008). Honey for nutrition and health: A review. Journal of the American College of Nutrition, 27(6). https://doi.org/10.1080/07315724.2008.10719745
Bonferroni, C. E. (1936). Teoria statistica delle classi e calcolo delle probabilità. Pubblicazioni Del R Istituto Superiore Di Scienze Economiche e Commerciali Di Firenze, 8.
Brodschneider, R., & Crailsheim, K. (2010). Nutrition and health in honey bees. Apidologie, 41(3). https://doi.org/10.1051/apido/2010012
Brodschneider, R., Moosbeckhofer, R., & Crailsheim, K. (2010). Surveys as a tool to record winter losses of honey bee colonies: A two year case study in Austria and South Tyrol. Journal of Apicultural Research, 49(1). https://doi.org/10.3896/IBRA.1.49.1.04
Brodschneider, R., Riessberger-Gallé, U., & Crailsheim, K. (2009). Flight performance of artificially reared honeybees (Apis mellifera). Apidologie, 40(4). https://doi.org/10.1051/apido/2009006
Brune, A. (2014). Symbiotic digestion of lignocellulose in termite guts. Nature Reviews Microbiology, 12(3). https://doi.org/10.1038/nrmicro3182
Carreck, N. L., Andree, M., Brent, C. S., Cox-Foster, D., Dade, H. A., Ellis, J. D., Hatjina, F., & van Englesdorp, D. (2013). Standard methods for Apis mellifera anatomy and dissection. Journal of Apicultural Research, 52(4). https://doi.org/10.3896/IBRA.1.52.4.03
Chopra, I., & Roberts, M. (2001). Tetracycline Antibiotics: Mode of Action, Applications, Molecular Biology, and Epidemiology of Bacterial Resistance. Microbiology and Molecular Biology Reviews, 65(2). https://doi.org/10.1128/mmbr.65.2.232-260.2001
Dadd, R. H. (1973). Insect nutrition: current developments and metabolic implications. Annual review of entomology, 18(381). https://doi.org/10.1146/annurev.en.18.010173.002121
Douglas, A. E. (1998). Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology, 43(17). https://doi.org/10.1146/annurev.ento.43.1.17
Douglas, A. E. (2017). The B vitamin nutrition of insects: the contributions of diet, microbiome and horizontally acquired genes. Current Opinion in Insect Science, 23(65). https://doi.org/10.1016/j.cois.2017.07.012
Douglas, A. E. (2018). Gut microbes alter the walking activity of fruit flies. Nature, 563(7731). https://doi.org/10.1038/d41586-018-07080-y
du Rand, E. E., Stutzer, C., Human, H., Pirk, C. W. W., & Nicolson, S. W. (2020). Antibiotic treatment impairs protein digestion in the honeybee, Apis mellifera. Apidologie, 51(1). https://doi.org/10.1007/s13592-019-00718-4
Duncan, S. H., Lobley, G. E., Holtrop, G., Ince, J., Johnstone, A. M., Louis, P., & Flint, H. J. (2008). Human colonic microbiota associated with diet, obesity and weight loss. International Journal of Obesity, 32(11). https://doi.org/10.1038/ijo.2008.155
EFSA. (2016). Panel Scientific opinion on assessing the health status of managed honeybee colonies (HEALTHY-B): a toolbox to facilitate harmonised data collection. EFSA Journal, 14(10). https://doi.org/10.2903/j.efsa.2016.4578
Frias, B. E. D., Barbosa, C. D., & Lourenço, A. P. (2016). Pollen nutrition in honey bees (Apis mellifera): impact on adult health. Apidologie, 47(1). https://doi.org/10.1007/s13592-015-0373-y
Fukuda, H., & Sekiguchi, K. (1996). Seasonal change of the honeybee worker longevity in Sapporo, North Japan, with notes on some factors affecting the life-span, Japanese Journal of Ecology, 16(5). https://doi.org/10.18960/seitai.16.5_206
Graves, S., Piepho, HP., Selzer, L., Dorai-Raj, S. (2019). multcompView: Visualizations of Paired Comparisons. R package version 0.1–8. https://CRAN.R-project.org/package=multcompView
Hayashi, A., Mikami, Y., Miyamoto, K., Kamada, N., Sato, T., Mizuno, S., Naganuma, M., Teratani, T., Aoki, R., Fukuda, S., Suda, W., Hattori, M., Amagai, M., Ohyama, M., & Kanai, T. (2017). Intestinal Dysbiosis and Biotin Deprivation Induce Alopecia through Overgrowth of Lactobacillus murinus in Mice. Cell Reports, 20(7). https://doi.org/10.1016/j.celrep.2017.07.057
Haydak, M. H. (1970). Honey Bee Nutrition 1. Annual Reviews of Entomology, 15(1). https://doi.org/10.1146/annurev.en.15.010170.001043
Haydak, M. H. (1935). Brood Rearing by Honeybees Confined to a Pure Carbohydrate Diet. Journal of Economic Entomology, 28(4). https://doi.org/10.1093/jee/28.4.657
Haydak, M. H., & Dietz, A. (1972). Cholesterol, pantothenic acid, pyridoxine and thiamine requirements of honeybees for brood rearing. Journal of Apicultural Research, 11(2). https://doi.org/10.1080/00218839.1972.11099707
Holm, S. (1979). A Simple Sequentially Rejective Multiple Test Procedure. Scandinavian Journal of Statistics, 6(2). http://www.jstor.org/stable/4615733
Huang, S.K., Csaki, T., Doublet, V., Dussaubat, C., Evans, J.D., Gajda, A.M., Gregorc, A., Hamilton, M.C., Kamler, M., Lecocq, A., Muz, M.N., Neumann, P., Özkirim, A., Schiesser, A., Sohr, A. R., Tanner,G., Tozkar, C, Ö., Williams, G. R., Wu, L., Zheng, H., & Chen, Y. P. (2014). Evaluation of Cage Designs and Feeding Regimes for Honey Bee (Hymenoptera: Apidae) Laboratory Experiments, Journal of Economic Entomology, 107(1). https://doi.org/10.1603/EC13213
Hothorn,T., Frank Bretz, F., & Westfall, P. (2008). Simultaneous Inference in General Parametric Models. Biometrical Journal, 50(3). 346-363
Jovanovic, N. M., Glavinic, U., Delic, B., Vejnovic, B., Aleksic, N., Mladjan, V., & Stanimirovic, Z. (2021). Plant-based supplement containing B-complex vitamins can improve bee health and increase colony performance. Preventive Veterinary Medicine, 190. https://doi.org/10.1016/j.prevetmed.2021.105322
Kešnerová, 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 Biology, 15(12). https://doi.org/10.1371/journal.pbio.2003467
Klein, S., Pasquaretta, C., He, X. J., Perry, C., Søvik, E., Devaud, J. M., Barron, A. B., & Lihoreau, M. (2019). Honey bees increase their foraging performance and frequency of pollen trips through experience. Scientific Reports, 9(1). https://doi.org/10.1038/s41598-019-42677-x
Köhler, A., Nicolson, S. W., & Pirk, C. W. W. (2013). A new design for honey bee hoarding cages for laboratory experiments. In Journal of Apicultural Research, 52(2). https://doi.org/10.3896/IBRA.1.52.2.03
Kosinski, M., Kassambara, A., & Biecek, P. (2020). Survminer: Drawing Survival Curves using “ggplot2.” In R package version 0.4.7.
Kwong, W. K., Engel, P., Koch, H., & Moran, N. A. (2014). Genomics and host specialization of honey bee and bumble bee gut symbionts. Proceedings of the National Academy of Sciences of the United States of America, 111(31). https://doi.org/10.1073/pnas.1405838111
Kwong, W. K., & Moran, N. A. (2016). Gut microbial communities of social bees. Nature Reviews Microbiology, 14(6). https://doi.org/10.1038/nrmicro.2016.43
Ludicke, J. C., & Nieh, J. C. (2020). Thiamethoxam impairs honey bee visual learning, alters decision times, and increases abnormal behaviors. Ecotoxicology and Environmental Safety, 193. https://doi.org/10.1016/j.ecoenv.2020.110367
Maes, P. W., Rodrigues, P. A. P., Oliver, R., Mott, B. M., & Anderson, K. E. (2016). Diet-related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honeybee (Apis mellifera). Molecular Ecology, 25(21). https://doi.org/10.1111/mec.13862
Marceau, T., Archer, C. R., Bulson, L., & Wilfert, L. (2021). Dose-dependent effects of antibiotic intake on Bombus terrestris (Linnaeus, 1758) dietary intake, survival and parasite infection prevalence. Journal of Invertebrate Pathology, 182. https://doi.org/10.1016/j.jip.2021.107580
Martinson, V. G., Moy, J., & Moran, N. A. (2012). Establishment of characteristic gut bacteria during development of the honeybee worker. Applied and Environmental Microbiology, 78(8). https://doi.org/10.1128/AEM.07810-11
Maurizo, A. (1954). Pollenernährung und Lebensvorgänge bei der Honigbiene (Apis mellifera L.). Landwirtsch. Jarh. Schweiz, 245.
Meyer, H. E., Willett, W. C., Fung, T. T., Holvik, K., & Feskanich, D. (2019). Association of high intakes of vitamins B6 and B12 from food and supplements with risk of hip fracture among Postmenopausal Women in the Nurses’ Health Study. JAMA Network Open, 2(5). https://doi.org/10.1001/jamanetworkopen.2019.3591
Naug, D. (2009). Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biological Conservation, 142(10). https://doi.org/10.1016/j.biocon.2009.04.007
Neukirch, A. (1982). Dependence of the life span of the honeybee (Apis mellifica) upon flight performance and energy consumption. Journal of Comparative Physiology, 146(1). https://doi.org/10.1007/BF00688714
Neumann, P., & Carreck, N. L. (2010). Honey bee colony losses. Journal of Apicultural Research, 49(1). https://doi.org/10.3896/IBRA.1.49.1.01
OECD (2017), Test No. 245: Honey Bee (Apis mellifera L.), Chronic Oral Toxicity Test (10-Day Feeding), OECD Guidelines for the Testing of Chemicals, Section 2, OECD Publishing, 9. https://doi.org/10.1787/9789264284081-en.
Phillips, W. E. J., Mills, J. H. L., Charbonneau, S. M., Tryphonas, L., Hatina, G. v., Zawidzka, Z., Bryce, F. R., & Munro, I. C. (1978). Subacute toxicity of pyridoxine hydrochloride in the beagle dog. Toxicology and Applied Pharmacology, 44(2). https://doi.org/10.1016/0041-008X(78)90194-1
Piepho, HP. (2004), An Algorithm for a Letter-Based Representation of All-Pairwise Comparisons, Journal of Computational and Graphical Statistics, 13(2). 456-466.
Pudasaini, R., Dhital, B., & Chaudhary, S. (2020). Nutritional requirement and its role on honeybee: a review. Journal of Agriculture and Natural Resources, 3(2). https://doi.org/10.3126/janr.v3i2.32544
Raymann, K., Shaffer, Z., & Moran, N. A. (2017). Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PloS Biology, 15(3). https://doi.org/10.1371/journal.pbio.2001861
R Core Team. (2008). R: a Language and Environment for Statistical Computing. In http://www.R-project.org/ (Vol. 2).
Retschnig, G., Rich, J., Crailsheim, K., Pfister, J., Perreten, V., & Neumann, P. (2021). You are what you eat: relative importance of diet, gut microbiota and nestmates for honey bee, Apis mellifera, worker health. Apidologie, 52(3). https://doi.org/10.1007/s13592-021-00851-z
Roulston, T. H., & Cane, J. H. (2000). Pollen nutritional content and digestibility for animals. Plant Systematics and Evolution, 222(1). https://doi.org/10.1007/BF00984102
Salem, H., Bauer, E., Strauss, A. S., Vogel, H., Marz, M., & Kaltenpoth, M. (2014). Vitamin supplementation by gut symbionts ensures metabolic homeostasis in an insect host. Proceedings of the Royal Society B: Biological Sciences, 281(1796). https://doi.org/10.1098/rspb.2014.1838
Sanhueza, E., Paredes-Osses, E., González, C. L., & García, A. (2015). Effect of pH in the survival of Lactobacillus salivarius strain UCO_979C wild type and the pH acid acclimated variant. Electronic Journal of Biotechnology, 18(5). https://doi.org/10.1016/j.ejbt.2015.06.005
Somerville, D. (2000). Honey bee nutrition and supplementary feeding, Agnote DAI/178, NSW Agriculture. Online: https://www.dpi.nsw.gov.au/__data/assets/pdf_file/0008/117494/honey-bee-nutrition-supplementary-feeding.pdf, (accessed 03.04.2021)
Standifer, L. N., Moeller, F. E., Kauffeld, N. M., Herbert, E. W., Jr., & Shimanuki, H. (1977). Supplemental Feeding of Honey Bee Colonies. United States Department of Agriculture, 413.
Suchail, S., Debrauwer, L., & Belzunces, L. P. (2004). Metabolism of imidacloprid in Apis mellifera. Pest Management Science, 60(3). https://doi.org/10.1002/ps.772
Tejerina, M. R., Cabana, M. J., & Benitez-Ahrendts, M. R. (2021). Strains of Lactobacillus spp. reduce chalkbrood in Apis mellifera. Journal of Invertebrate Pathology, 178. https://doi.org/10.1016/j.jip.2020.107521
Therneau, T. M. (2021). Survival: A Package for Survival Analysis in R. R Package Version 2.38.
Therneau, T. M., & Grambsch, P. M. (2000). The Cox Model BT – Modeling Survival Data: Extending the Cox Model. In Statistics for Biology and Health.
Titcomb, T. J., & Tanumihardjo, S. A. (2019). Global Concerns with B Vitamin Statuses: Biofortification, Fortification, Hidden Hunger, Interactions, and Toxicity. Comprehensive Reviews in Food Science and Food Safety, 18(6). https://doi.org/10.1111/1541-4337.12491
van Engelsdorp, D., Speybroeck, N., Evans, J. D., Nguyen, B. K., Mullin, C., Frazier, M., Frazier, J., Cox-Foster, D., Chen, Y., Tarpy, D. R., Haubruge, E., Pettis, J. S., & Saegerman, C. (2010). Weighing risk factors associated with bee colony collapse disorder by classification and regression tree analysis. Journal of Economic Entomology, 103(5). https://doi.org/10.1603/EC09429
Vásquez, 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). https://doi.org/10.1371/journal.pone.0033188
Vásquez, A., & Olofsson, T. C. (2009). The lactic acid bacteria involved in the production of bee pollen and bee bread. Journal of Apicultural Research, 48(3). https://doi.org/10.3896/IBRA.1.48.3.07
Williams, G. R., Alaux, C., Costa, C., Csáki, T., Doublet, V., Eisenhardt, D., Fries, I., Kuhn, R., McMahon, D. P., Medrzycki, P., Murray, T. E., Natsopoulou, M. E., Neumann, P., Oliver, R., Paxton, R. J., Pernal, S. F., Shutler, D., Tanner, G., van der Steen, J. J. M., & Brodschneider, R. (2013). Standard methods for maintaining adult Apis mellifera in cages under in vitro laboratory conditions. Journal of Apicultural Research, 52(1). https://doi.org/10.3896/IBRA.1.52.1.04
Winston, Mark L. (1991). The biology of the honey bee. Cambridge, Mass: Harvard University Press, Cambridge, Massachusetts
Xu, S., Jiang, L., Qiao, G., & Chen, J. (2020). The Bacterial Flora Associated with the Polyphagous Aphid Aphis gossypii Glover (Hemiptera: Aphididae) Is Strongly Affected by Host Plants. Microbial Ecology, 79(4). https://doi.org/10.1007/s00248-019-01435-2