The effect of carbohydrate sources: Sucrose, invert sugar and components of mānuka honey, on core bacteria in the digestive tract of adult honey bees (Apis mellifera)

Autoři: Michelle A. Taylor aff001;  Alastair W. Robertson aff002;  Patrick J. Biggs aff003;  Kate K. Richards aff005;  Daniel F. Jones aff006;  Shanthi G. Parkar aff007
Působiště autorů: Bee Biology & Productivity, Productive Biodiversity and Pollination, The New Zealand Institute for Plant and Food Research Limited, Hamilton, New Zealand aff001;  Wildlife & Ecology, School of Agriculture and Environment, Massey University, Palmerston North, New Zealand aff002;  Molecular Epidemiology & Public Health Laboratory, Infectious Disease Research Centre, School of Veterinary Science, Massey University, Palmerston North, New Zealand aff003;  Bioinformatics and Statistics Group, School of Fundamental Sciences, Massey University, Palmerston North, New Zealand aff004;  Statistical Science, Data Science, The New Zealand Institute for Plant and Food Research Limited, Auckland, New Zealand aff005;  Bioinformatics, Molecular & Digital Breeding, The New Zealand Institute for Plant and Food Research Limited, Auckland, New Zealand aff006;  Microbiome & Metabolism, Food Nutrition & Health, The New Zealand Institute for Plant and Food Research Limited, Palmerston North, New Zealand aff007
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pone.0225845


Bacteria within the digestive tract of adult honey bees are likely to play a key role in the digestion of sugar-rich foods. However, the influence of diet on honey bee gut bacteria is not well understood. During periods of low floral abundance, beekeepers often supplement the natural sources of carbohydrate that honey bees collect, such as nectar, with various forms of carbohydrates such as sucrose (a disaccharide) and invert sugar (a mixture of the monosaccharides glucose and fructose). We compared the effect of these sugar supplements on the relative abundance of bacteria in the gut of bees by feeding bees from a single colony, two natural diets: mānuka honey, a monofloral honey with known antibacterial properties, and a hive diet; and artificial diets of invert sugar, sucrose solution, and sucrose solutions containing synthesised compounds associated with the antibacterial properties of mānuka honey. 16S ribosomal RNA (rRNA)-based sequencing showed that dietary regimes containing mānuka honey, sucrose and invert sugar did not alter the relative abundance of dominant core bacteria after 6 days of being fed these diets. However, sucrose-rich diets increased the relative abundances of three sub-dominant core bacteria, Rhizobiaceae, Acetobacteraceae, and Lactobacillus kunkeei, and decreased the relative abundance of Frischella perrara, all which significantly altered the bacterial composition. Acetogenic bacteria from the Rhizobiaceae and Acetobacteraceae families increased two- to five-fold when bees were fed sucrose. These results suggest that sucrose fuels the proliferation of specific low abundance primary sucrose-feeders, which metabolise sugars into monosaccharides, and then to acetate.

Klíčová slova:

Bacteria – Bees – Carbohydrates – Diet – Honey – Honey bees – Lactobacillus – Sucrose


1. Southwick EE, Southwick L. Estimating the economic value of honey bees (Hymenoptera: Apidae) as agricultural pollinators in the United States. Journal of Economic Entomology. 1992;85(3):621–33.

2. Morse RA, Calderone NW. The value of honey bees as pollinators of US crops in 2000. Bee Culture. 2000;128(3):1–15.

3. Free JB. Insect Pollination of Crops. London, New York: Academic Press; 1970. 544 p.

4. Gallai N, Salles J-M, Settele J, Vaissière BE. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics. 2009;68(3):810–21.

5. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE. Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution. 2010;25(6):345–53.

6. Severson D, Erickson E. Honey bee (Hymenoptera: Apidae) colony performance in relation to supplemental carbohydrates. Journal of Economic Entomology. 1984;77(6):1473–8.

7. Human H, Nicolson SW. Nutritional content of fresh, bee-collected and stored pollen of Aloe greatheadii var. davyana (Asphodelaceae). Phytochemistry. 2006;67(14):1486–92. doi: 10.1016/j.phytochem.2006.05.023 16808932

8. Saraiva MA, Zemolin APP, Franco JL, Boldo JT, Stefenon VM, Triplett EW, et al. Relationship between honeybee nutrition and their microbial communities. Antonie van Leeuwenhoek. 2015:1–13.

9. Wykes GR. An investigation of the sugars present in the nectar of flowers of various species. New Phytologist. 1952;51:210–5.

10. Chalcoff VR, Aizen MA, Galetto L. Nectar concentration and composition of 26 species from the temperate forest of South America. Annals of Botany. 2005;97(3):413–21. doi: 10.1093/aob/mcj043 16373370

11. White JW, Riethof ML, Subers MH, Kushnir I. Composition of American honeys: Technical Bulletin No. 1261: United States Department of Agriculture; 1962. 124 p.

12. Doner LW. The sugars of honey—a review. Journal of the Science of Food and Agriculture. 1977;28(5):443–56. doi: 10.1002/jsfa.2740280508 875373

13. Baxter NT, Schmidt AW, Venkataraman A, Kim KS, Waldron C, Schmidt TM. Dynamics of Human Gut Microbiota and Short-Chain Fatty Acids in Response to Dietary Interventions with Three Fermentable Fibers. mBio. 2019;10(1):e02566–18. doi: 10.1128/mBio.02566-18 30696735

14. Barker RJ, Lehner Y. Laboratory comparison of high fructose corn syrup, grape syrup, honey, and sucrose syrup as maintenance food for caged honey bees. Apidologie. 1978;9(2):111–6.

15. Graham JM. The hive and the honey bee: Dadant & Sons; 1992.

16. Alaux C, Brunet J-L, Dussaubat C, Mondet F, Tchamitchan S, Cousin M, et al. Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environmental Microbiology. 2010;12(3):774–82. doi: 10.1111/j.1462-2920.2009.02123.x 20050872

17. Wahl O, Ulm K. Influence of pollen feeding and physiological condition on pesticide sensitivity of the honey bee Apis mellifera carnica. Oecologia. 1983;59(1):106–28. doi: 10.1007/BF00388082 25024157

18. Wheeler MM, Robinson GE. Diet-dependent gene expression in honey bees: honey vs. sucrose or high fructose corn syrup. Scientific Reports. 2014;4.

19. Sangüesa G, Shaligram S, Akther F, Roglans N, Laguna JC, Rahimian R, et al. Type of supplemented simple sugar, not merely calorie intake, determines adverse effects on metabolism and aortic function in female rats. American Journal of Physiology-Heart and Circulatory Physiology. 2016;312(2):H289–H304. doi: 10.1152/ajpheart.00339.2016 27923787

20. Guarner F. The intestinal flora in inflammatory bowel disease: normal or abnormal? Current Opinion in Gastroenterology. 2005;21(4):414–8. 15930980

21. Colman DR, Toolson EC, Takacs‐Vesbach C. Do diet and taxonomy influence insect gut bacterial communities? Molecular Ecology. 2012;21(20):5124–37. doi: 10.1111/j.1365-294X.2012.05752.x 22978555

22. Maes PW, Rodrigues PA, Oliver R, Mott BM, Anderson KE. Diet‐related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honeybee (Apis mellifera). Molecular Ecology. 2016;25(21):5439–50. doi: 10.1111/mec.13862 27717118

23. Jones JC, Fruciano C, Hildebrand F, Al Toufalilia H, Balfour NJ, Bork P, et al. Gut microbiota composition is associated with environmental landscape in honey bees. Ecology and Evolution. 2018;8(1):441–51. doi: 10.1002/ece3.3597 29321884

24. Rothman JA, Carroll MJ, Meikle WG, Anderson KE, McFrederick QS. Longitudinal effects of supplemental forage on the honey bee (Apis mellifera) microbiota and inter-and intra-colony variability. Microbial Ecology. 2018;76(3):814–24. doi: 10.1007/s00248-018-1151-y 29397399

25. Kwong WK, Moran NA. Gut microbial communities of social bees. Nature Reviews Microbiology. 2016;14(6):374–84. doi: 10.1038/nrmicro.2016.43 27140688

26. Ludvigsen J, Rangberg A, Avershina E, Sekelja M, Kreibich C, Amdam G, et al. Shifts in the midgut/pyloric microbiota composition within a honey bee apiary throughout a season. Microbes and Environments. 2015;30(3):235. doi: 10.1264/jsme2.ME15019 26330094

27. Kwong WK, Moran NA. Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order ‘Enterobacteriales’ of the Gammaproteobacteria. International Journal of Systematic and Evolutionary Microbiology. 2013;63(6):2008–18.

28. Babendreier D, Joller D, Romeis J, Bigler F, Widmer F. Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. Federation of European Microbiological Societies: Microbiology Ecology. 2007;59(3):600–10. doi: 10.1111/j.1574-6941.2006.00249.x 17381517

29. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA. A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology. 2011;20(3):619–28. doi: 10.1111/j.1365-294X.2010.04959.x 21175905

30. Bottacini F, Milani C, Turroni F, Sánchez B, Foroni E, Duranti S, et al. Bifidobacterium asteroides PRL2011 genome analysis reveals clues for colonization of the insect gut. Plos One. 2012;7(9):e44229. doi: 10.1371/journal.pone.0044229 23028506

31. Engel P, Kwong WK, Moran NA. Frischella perrara gen. nov., sp. nov., a gammaproteobacterium isolated from the gut of the honeybee, Apis mellifera. International Journal of Systematic and Evolutionary Microbiology. 2013;63:3646–51. doi: 10.1099/ijs.0.049569-0 23606484

32. Kešnerová L, Moritz R, Engel P. Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria. International Journal of Systematic and Evolutionary Microbiology. 2016;66(1):414–21. doi: 10.1099/ijsem.0.000736 26537852

33. Corby-Harris V, Snyder LA, Schwan MR, Maes P, McFrederick QS, Anderson KE. Origin and effect of Acetobacteraceae Alpha 2.2 in honey bee larvae and description of Parasaccharibacter apium, gen. nov., sp. nov. Applied and Environmental Microbiology. 2014:2043–14.

34. Yu R-Y, Martin WF. Symbiotic Associations: All About Chemistry. In: Hurst C, editor. The Mechanistic Benefits of Microbial Symbionts. 2: Springer, Cham; 2016. p. 3–11.

35. Vojvodic S, Rehan SM, Anderson KE. Microbial Gut diversity of Africanized and European honey Bee larval instars. Plos One. 2013;8(8):e72106. doi: 10.1371/journal.pone.0072106 23991051

36. Zheng H, Powell JE, Steele MI, Dietrich C, Moran NA. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling. Proceedings of the National Academy of Sciences. 2017;114(18):4775–80.

37. Martinson VG, Moy J, Moran NA. Establishment of characteristic gut bacteria during development of the honeybee worker. Applied and Environmental Microbiology. 2012;78(8):2830–40. doi: 10.1128/AEM.07810-11 22307297

38. Powell JE, Martinson VG, Urban-Mead K, Moran NA. Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Applied and Environmental Microbiology. 2014;80(23):7378–87. doi: 10.1128/AEM.01861-14 25239900

39. Dillon R, Dillon V. The gut bacteria of insects: nonpathogenic interactions. Annual Reviews in Entomology. 2004;49(1):71–92.

40. Engel P, Moran NA. The gut microbiota of insects–diversity in structure and function. Federation of European Microbiological Societies: Microbiology Reviews. 2013;37(5):699–735.

41. Lee FJ, Rusch DB, Stewart FJ, Mattila HR, Newton IL. Saccharide breakdown and fermentation by the honey bee gut microbiome. Environmental Microbiology. 2015;17(3):796–815. doi: 10.1111/1462-2920.12526 24905222

42. Zheng H, Nishida A, Kwong WK, Koch H, Engel P, Steele MI, et al. Metabolism of toxic sugars by strains of the bee gut symbiont Gilliamella apicola. MBio. 2016;7(6):e01326–16. doi: 10.1128/mBio.01326-16 27803186

43. Wang M, Zhao W-Z, Xu H, Wang Z-W, He S-Y. Bacillus in the guts of honey bees (Apis mellifera; Hymenoptera: Apidae) mediate changes in amylase values. European Journal of Entomology. 2015;112(4):619–24.

44. Molan PC. The antibacterial activity of honey. 2. Variation in the potency of the antibacterial activity. Bee World. 1992;73(2):59–76.

45. Kwakman PH, te Velde AA, de Boer L, Speijer D, Vandenbroucke-Grauls CM, Zaat SA. How honey kills bacteria. Federation of American Societies for Experimental Biology Journal. 2010;24(7):2576–82. doi: 10.1096/fj.09-150789 20228250

46. Chepulis L, Francis E. The glycaemic index of Mānuka honey. e-SPEN Journal. 2013;8(1):e21–e4.

47. Weston RJ, Brocklebank LK. The oligosaccharide composition of some New Zealand honeys. Food Chemistry. 1999;64(1):33–7.

48. Moniruzzaman M, Sulaiman SA, Khalil MI, Gan SH. Evaluation of physicochemical and antioxidant properties of sourwood and other Malaysian honeys: a comparison with mānuka honey. Chemistry Central Journal. 2013;7(1):138.

49. Willix DJ, Molan PC, Harfoot CJ. A comparison of the sensitivity of wound-infecting species of bacteria to the antibacterial activity of manuka honey and other honey. Journal of Applied Bacteriology. 1992;73:388–94. doi: 10.1111/j.1365-2672.1992.tb04993.x 1447054

50. Mavric E, Wittmann S, Barth G, Henle T. Identification and quantification of methylglyoxal as the dominant antibacterial constituent of Manuka (Leptospermum scoparium) honeys from New Zealand. Molecular Nutrition and Food Research. 2008;52(4):483–9. doi: 10.1002/mnfr.200700282 18210383

51. Majtan J, Klaudiny J, Bohova J, Kohutova L, Dzurova M, Sediva M, et al. Methylglyoxal-induced modifications of significant honeybee proteinous components in mānuka honey: possible therapeutic implications. Fitoterapia. 2012;83(4):671–7. doi: 10.1016/j.fitote.2012.02.002 22366273

52. Adams CJ, Manley-Harris M, Molan PC. The origin of methylglyoxal in New Zealand mānuka (Leptospermum scoparium) honey. Carbohydrate Research. 2009;344(8):1050–3. doi: 10.1016/j.carres.2009.03.020 19368902

53. Atrott J, Haberlau S, Henle T. Studies on the formation of methylglyoxal from dihydroxyacetone in Manuka (Leptospermum scoparium) honey. Carbohydrate Research. 2012;361:7–11. doi: 10.1016/j.carres.2012.07.025 22960208

54. Haydak MH. Honey bee nutrition. Annual Review of Entomology. 1970;15(1):143–56.

55. Mannina L, Sobolev AP, Coppo E, Di Lorenzo A, Nabavi SM, Marchese A, et al. Antistaphylococcal activity and metabolite profiling of mānuka honey (Leptospermum scoparium L.) after in vitro simulated digestion. Food and Function. 2016;7(3):1664–70. doi: 10.1039/c5fo01409c 26948514

56. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79(17):5112–20. doi: 10.1128/AEM.01043-13 23793624

57. Aronesty E. ea-utils: Command-line tools for processing biological sequencing data; 2011.

58. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nature Methods. 2010;7(5):335. doi: 10.1038/nmeth.f.303 20383131

59. Kuczynski J, Stombaugh J, Walters WA, González A, Caporaso JG, Knight R. Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Current protocols in microbiology. 2012;27(1):1E. 5.1–E. 5.20.

60. Dhariwal A, Chong J, Habib S, King IL, Agellon LB, Xia J. MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Research. 2017;45(W1):W180–W8. doi: 10.1093/nar/gkx295 28449106

61. Anderson MJ. A new method for non‐parametric multivariate analysis of variance. Austral Ecology. 2001;26(1):32–46.

62. R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing: ISBN 3-900051-07-0: URL; 2018.

63. Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. Journal of Statistical Software. 2014;67(1):1–48.

64. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. Vegan: Community Ecology Package. R package version 2.5–3. 2018.

65. Engel P, Bartlett KD, Moran NA. The bacterium Frischella perrara causes scab formation in the gut of its honeybee host. mBio. 2015;6(3):e00193–15. doi: 10.1128/mBio.00193-15 25991680

66. Kwakman PH, Van den Akker JP, Güçlü A, Aslami H, Binnekade JM, de Boer L, et al. Medical-grade honey kills antibiotic-resistant bacteria in vitro and eradicates skin colonization. Clinical Infectious Diseases. 2008;46(11):1677–82. doi: 10.1086/587892 18433338

67. Olofsson TC, Alsterfjord M, Nilson B, Butler È, Vásquez A. Lactobacillus apinorum sp. nov., Lactobacillus mellifer sp. nov., Lactobacillus mellis sp. nov., Lactobacillus melliventris sp. nov., Lactobacillus kimbladii sp. nov., Lactobacillus helsingborgensis sp. nov. and Lactobacillus kullabergensis sp. nov., isolated from the honey stomach of the honeybee Apis mellifera. International Journal of Systematic and Evolutionary Microbiology. 2014;64:3109–19. doi: 10.1099/ijs.0.059600-0 24944337

68. Olofsson TC, Vásquez A. Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Current Microbiology. 2008;57(4):356–63. doi: 10.1007/s00284-008-9202-0 18663527

69. Kersters K, Lisdiyanti P, Komagata K, Swings J. The family acetobacteraceae: the genera acetobacter, acidomonas, asaia, gluconacetobacter, gluconobacter, and kozakia. The prokaryotes: Springer; 2006. p. 163–200.

70. Crotti E, Rizzi A, Chouaia B, Ricci I, Favia G, Alma A, et al. Acetic acid bacteria, newly emerging symbionts of insects. Applied and Environmental Microbiology. 2010;76(21):6963–70. doi: 10.1128/AEM.01336-10 20851977

71. Mitraka E, Stathopoulos S, Siden-Kiamos I, Christophides GK, Louis C. Asaia accelerates larval development of Anopheles gambiae. Pathogens and global health. 2013;107(6):305–11. doi: 10.1179/2047773213Y.0000000106 24091152

72. Ryu J-H, Kim S-H, Lee H-Y, Bai JY, Nam Y-D, Bae J-W, et al. Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science. 2008;319(5864):777–82. doi: 10.1126/science.1149357 18218863

73. Zhou G-c, Wang Y, Zhai S, Ge F, Liu Z-h, Dai Y-j, et al. Biodegradation of the neonicotinoid insecticide thiamethoxam by the nitrogen-fixing and plant-growth-promoting rhizobacterium Ensifer adhaerens strain TMX-23. Applied microbiology and biotechnology. 2013;97(9):4065–74. doi: 10.1007/s00253-012-4638-3 23274958

74. Geddes BA, Oresnik IJ. The Mechanism of Symbiotic Nitrogen Fixation. In: Hurst C.(eds) The Mechanistic Benefits of Microbial Symbionts. Advances in Environmental Microbiology, vol 2. Springer, Cham. 2016.

75. Rogel MA, Hernández-Lucas I, Kuykendall LD, Balkwill DL, Martinez-Romero E. Nitrogen-fixing nodules with Ensifer adhaerens harboring Rhizobium tropici symbiotic plasmids. Applied and Environmental Microbiology. 2001;67(7):3264–8. doi: 10.1128/AEM.67.7.3264-3268.2001 11425750

76. McFrederick QS, Wcislo WT, Taylor DR, Ishak HD, Dowd SE, Mueller UG. Environment or kin: whence do bees obtain acidophilic bacteria? Molecular Ecology. 2012;21(7):1754–68. doi: 10.1111/j.1365-294X.2012.05496.x 22340254

77. Neveling DP, Endo A, Dicks LM. Fructophilic Lactobacillus kunkeei and Lactobacillus brevis isolated from fresh flowers, bees and bee-hives. Current Microbiology. 2012;65(5):507–15. doi: 10.1007/s00284-012-0186-4 22797888

78. Anderson KE, Sheehan TH, Mott BM, Maes P, Snyder L, Schwan MR, et al. Microbial ecology of the hive and pollination landscape: bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera). Plos One. 2013;8(12):83125.

79. Asama T, Arima TH, Gomi T, Keishi T, Tani H, Kimura Y, et al. Lactobacillus kunkeei YB 38 from honeybee products enhances IgA production in healthy adults. Journal of Applied Microbiology. 2015;119(3):818–26. doi: 10.1111/jam.12889 26121394

80. Rortais A, Arnold G, Halm M-P, Touffet-Briens F. Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie. 2005;36(1):71–83.

81. Bonilla-Rosso G, Engel P. Functional roles and metabolic niches in the honey bee gut microbiota. Current Opinion in Microbiology. 2018;43:69–76. doi: 10.1016/j.mib.2017.12.009 29309997

82. Fukuda H, Sekiguchi K. Seasonal change of the honeybee worker longevity in Sapporo, North Japan, with notes on some factors affecting the life-span. Japanese Journal of Ecology. 1966;16(5):206–12.

83. Wei G, Lai Y, Wang G, Chen H, Li F, Wang S. Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality. Proceedings of the National Academy of Sciences. 2017;114(23):5994–9.

84. Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC, et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host and Microbe. 2007;2(2):119–29. doi: 10.1016/j.chom.2007.06.010 18005726

85. Crailsheim K. Intestinal transport of sugars in the honeybee (Apis mellifera L.). Journal of insect physiology. 1988;34(9):839–45.

86. Nicolson SW, Human H. Bees get a head start on honey production. Biology Letters. 2008;4(3):299–301. doi: 10.1098/rsbl.2008.0034 18364310

87. Terra WR, Ferreira C. Insect digestive enzymes: properties, compartmentalization and function. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry. 1994;109(1):1–62.

88. Huang Z. Honey bee nutrition. American Bee Journal. 2010;150(8):773–6.

89. Free J, editor Hypopharyngeal gland development and division of labour in honey-bee (Apis mellifera L.) colonies. Proceedings of the Royal Entomological Society of London Series A, General Entomology; 1961: Wiley Online Library.

90. Brodschneider R, Crailsheim K. Nutrition and health in honey bees. Apidologie. 2010;41(3):278–94.

91. Knecht D, Kaatz H. Patterns of larval food production by hypopharyngeal glands in adult worker honey bees. Apidologie. 1990;21(5):457–68.

92. Peng Y-S, Nasr M, Marston JM, Fang Y. The digestion of dandelion pollen by adult worker honeybees. Physiological Entomology. 1985;10(1):75–82.

93. Kešnerová L, Mars RAT, Ellegaard KM, Troilo M, Sauer U, Engel P. Disentangling metabolic functions of bacteria in the honey bee gut. PLOS Biology. 2017;15(12):e2003467. doi: 10.1371/journal.pbio.2003467 29232373

94. Perry RJ, Peng L, Barry NA, Cline GW, Zhang D, Cardone RL, et al. Acetate mediates a microbiome–brain–β-cell axis to promote metabolic syndrome. Nature. 2016;534(7606):213. doi: 10.1038/nature18309 27279214

95. Kalapos MP. The tandem of free radicals and methylglyoxal. Chemico-biological interactions. 2008;171(3):251–71. doi: 10.1016/j.cbi.2007.11.009 18164697

96. Lee FJ, Miller KI, McKinlay JB, Newton IL. Differential carbohydrate utilization and organic acid production by honey bee symbionts. FEMS Microbiology Ecology. 2018;94(8):fiy113.

97. Nagpal S, Haque MM, Singh R, Mande S. iVikodak–A platform and standard workflow for inferring, analyzing, comparing, and visualizing the functional potential of microbial communities. Frontiers in Microbiology. 2019;9:3336. doi: 10.3389/fmicb.2018.03336 30692979

Článok vyšiel v časopise


2019 Číslo 12