Publisher logo
Sign Up
Jordan Journal of Applied Science-Natural Science Series
Submit Manuscript
Applied Science Private University

Volume Volume 17, 2023 · Issue 1 · Open Access · Double-blind Peer-review

Submit an articleJournal homepage

Hypothesis

Examining the Effect of Lactic Acid Producing Bacteria on Honey Quality and Quantity

Shaymaa B. Abdulrazzaq1, Sawsan Abu Jamma’ah2, Anfal AL-Dalaeen3, Mahmoud Jaber4, Samar Sabri Qaddoumi5, Mohammad A. A. AL-Najjar6 & Muna Barakat7

1 Department of Pharmaceutics and Pharmaceutical Sciences, Faculty of Pharmacy, Applied Science Private University, Amman, Jordan.

2 The Jubilee Institute, Amman, Jordan.

3 Applied Science Private University

Published: 30 Dec 2023

https://doi.org/10.35192/jjoas-n.v17i1.1504
Download PDF
Abstract

Background: Honeybees play a pivotal role in the sustainability of ecosystems and biodiversity. Various environmental problems have affected the most significant pollinators—honeybees. Currently, many challenges are facing honeybee health, and lactic acid-producing bacteria, naturally found in honeybees' gut microbiota, could be used to enhance honey production and quality. This study aimed to examine the effect of using lactic acid-producing bacterial probiotics as a supplement in honeybee food on honey quality and quantity compared to unsupplemented honeybees.

Methods: Probiotic supplements (Lactobacillus reuteri, Lactobacillus helveticus, Lactobacillus bulgaricus, Lactobacillus acidophilus, and Bifidobacterium bifidum) for honeybees were prepared in three different forms (supernatant, pellet, and direct feeding probiotic) with a control group consuming only standard honeybee food (water with sugar). After the feeding process, honey samples were collected and analyzed for production rate (amount), proximate analysis (including HMF, ash, moisture, mineral content), and antioxidant content (flavonoid and phenolic levels).

Results: Our study showed that supplementing honeybee food resulted in an overall increase in honey production (p < 0.0001), especially in the supernatant group, which had a 147% increase. Phenolic content showed higher values overall, with particularly elevated mineral content in honeybees supplemented with the supernatant of probiotics only.

Conclusion: These results are expected to positively influence honeybee health and increase stress tolerance and disease resistance in the honeybee population. Additionally, an enhanced quality of honey produced could potentially be used as a supplemental food in the form of nutraceuticals to address nutrient deficiencies in humans.

KeywordsHoneybeesLactic acidProbioticsHoney QualityQuantity

License

Journal License

This work is licensed under a Creative Commons Attribution 4.0 International license

References

  1. Hung KJ, Kingston JM, Albrecht M, Holway DA, Kohn JR. The worldwide importance of honey bees as pollinators in natural habitats. Proc Biol Sci. 2018;285(1870).
  2. Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science. 2013;339(6127):1608-11.
  3. Brown MJF, Paxton RJ. The conservation of bees: a global perspective. Apidologie. 2009;40(3):410-6.
  4. Chmiel JA, Daisley BA, Pitek AP, Thompson GJ, Reid G. Understanding the Effects of Sublethal Pesticide Exposure on Honey Bees: A Role for Probiotics as Mediators of Environmental Stress. Frontiers in Ecology and Evolution. 2020;8.
  5. Memmott J, Craze PG, Waser NM, Price MV. Global warming and the disruption of plant–pollinator interactions. Ecology Letters. 2007;10(8):710-7.
  6. Franck P, Garnery L, Solignac M, Cornuet JM. THE ORIGIN OF WEST EUROPEAN SUBSPECIES OF HONEYBEES (APIS MELLIFERA): NEW INSIGHTS FROM MICROSATELLITE AND MITOCHONDRIAL DATA. Evolution. 1998;52(4):1119-34.
  7. Stout JC, Morales CL. Ecological impacts of invasive alien species on bees. Apidologie. 2009;40(3):388-409.
  8. Paudel YP, Mackereth R, Hanley R, Qin W. Honey bees (Apis mellifera L.) and pollination issues: Current status, impacts, and potential drivers of decline. Journal of Agricultural Science. 2015;7(6):93.
  9. Le Conte Y, Navajas M. Climate change: impact on honey bee populations and diseases. Revue Scientifique et Technique-Office International des Epizooties. 2008;27(2):499-510.
  10. Eteraf-Oskouei T, Najafi M. Traditional and modern uses of natural honey in human diseases: a review. Iran J Basic Med Sci. 2013;16(6):731-42.
  11. Ajibola A, Chamunorwa JP, Erlwanger KH. Nutraceutical values of natural honey and its contribution to human health and wealth. Nutrition & Metabolism. 2012;9(1):61.
  12. Viuda‐Martos M, Ruiz‐Navajas Y, Fernández‐López J, Pérez‐Álvarez J. Functional properties of honey, propolis, and royal jelly. Journal of food science. 2008;73(9):R117-R24.
  13. Crittenden AN. The importance of honey consumption in human evolution. Food and Foodways. 2011;19(4):257-73.
  14. Arredondo D, Castelli L, Porrini MP, Garrido PM, Eguaras MJ, Zunino P, et al. Lactobacillus kunkeei strains decreased the infection by honey bee pathogens Paenibacillus larvae and Nosema ceranae. Beneficial microbes. 2018;9(2):279-90.
  15. Wu J, Lang H, Mu X, Zhang Z, Su Q, Hu X, et al. Honey bee genetics shape the bee gut microbiota at the strain level. 2022.
  16. Alonso-Salces RM, Cugnata NM, Guaspari E, Pellegrini MC, Aubone I, De Piano FG, et al. Natural strategies for the control of Paenibacillus larvae, the causative agent of American foulbrood in honey bees: a review. Apidologie. 2017;48:387-400.
  17. Audisio MC. Gram-positive bacteria with probiotic potential for the Apis mellifera L. honey bee: the experience in the northwest of Argentina. Probiotics and antimicrobial proteins. 2017;9:22-31.
  18. Ramos OY, Basualdo M, Libonatti C, Vega MF. Current status and application of lactic acid bacteria in animal production systems with a focus on bacteria from honey bee colonies. Journal of applied microbiology. 2020;128(5):1248-60.
  19. Motta EV, Powell JE, Leonard SP, Moran NA. Prospects for probiotics in social bees. Philosophical Transactions of the Royal Society B. 2022;377(1853):20210156.
  20. Kim C, Kim JM, Choi H, Choi YS, Jin BR, Lee KS, et al. Analysis of the gut microbiome of susceptible and resistant honeybees (Apis cerana) against sacbrood virus disease. Journal of Applied Entomology. 2022;146(9):1078-86.
  21. Al-Waili NS, Salom K, Butler G, Al Ghamdi AA. Honey and microbial infections: a review supporting the use of honey for microbial control. Journal of medicinal food. 2011;14(10):1079-96.
  22. Dong Z-X, Tang Q-H, Li W-L, Wang Z-W, Li X-J, Fu C-M, et al. Honeybee (Apis mellifera) resistance to deltamethrin exposure by modulating the gut microbiota and improving immunity. Environmental Pollution. 2022;314:120340.
  23. Nixon M. Preliminary world maps of honeybee diseases and parasites. Bee World. 1982;63(1):23-42.
  24. Hammes WP, Hertel C. The genera lactobacillus and carnobacterium. The prokaryotes. 2006;4:320-403.
  25. Hotel ACP, Cordoba A. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Prevention. 2001;5(1):1-10.
  26. Vásquez A, Olofsson TC, Sammataro D. A scientific note on the lactic acid bacterial flora in honeybees in the USA–A comparison with bees from Sweden. Apidologie. 2009;40(1):26-8.
  27. 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;57:356-63.
  28. Olofsson TC, Vásquez A, Sammataro D, Macharia J. A scientific note on the lactic acid bacterial flora within the honeybee subspecies Apis mellifera (Buckfast), A. m. scutellata, A. m. mellifera, and A. m. monticola. Apidologie. 2011;42:696-9.
  29. OLOFSSON T, VASQUEZ A, Sammataro D. A scientific note on the lactic acid bacterial flora discovered in the honey stomach of Swedish honey bees-a continuing study on honey bees in the USA. Apidologie. 2009;40:26-8.
  30. Forsgren E, Olofsson TC, Vásquez A, Fries I. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie. 2010;41(1):99-108.
  31. Ng CM, Reuter WM. Analysis of Sugars in Honey Using the PerkinElmer Altus HPLC System with RI Detection. PerkinElmer, Inc. 2015;1(1).
  32. Singleton VL, Orthofer R, Lamuela-Raventós RM. [14] Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent.  Methods in enzymology. 299: Elsevier; 1999. p. 152-78.
  33. Arvouet-Grand A, Vennat B, Pourrat A, Legret P. Standardization of propolis extract and identification of principal constituents. Journal de pharmacie de Belgique. 1994;49(6):462-8.
  34. Kaznowski A, Szymas B, Jazdzinska E, Kazimierczak M, Paetz H, Mokracka J. The effects of probiotic supplementation on the content of intestinal microflora and chemical composition of worker honey bees (Apis mellifera). Journal of apicultural research. 2005;44(1):10-4.
  35. Iorizzo M, Letizia F, Ganassi S, Testa B, Petrarca S, Albanese G, et al. Functional Properties and Antimicrobial Activity from Lactic Acid Bacteria as Resources to Improve the Health and Welfare of Honey Bees. Insects. 2022;13(3):308.
  36. Audisio MC. Gram-Positive Bacteria with Probiotic Potential for the Apis mellifera L. Honey Bee: The Experience in the Northwest of Argentina. Probiotics and Antimicrobial Proteins. 2017;9(1):22-31.
  37. Tlak Gajger I, Vlainić J, Šoštarić P, Prešern J, Bubnič J, Smodiš Škerl MI. Effects on Some Therapeutical, Biochemical, and Immunological Parameters of Honey Bee (Apis mellifera) Exposed to Probiotic Treatments, in Field and Laboratory Conditions. Insects. 2020;11(9):638.
  38. Fanciotti MN, Tejerina M, Benítez-Ahrendts MR, Audisio MC. Honey yield of different commercial apiaries treated with Lactobacillus salivarius A3iob, a new bee-probiotic strain. Beneficial microbes. 2018;9(2):291-8.
  39. Pietropaoli M, Carpana E, Milito M, Palazzetti M, Guarducci M, Croppi S, et al. Use of Lactobacillus plantarum in preventing clinical cases of American and European foulbrood in central Italy. Applied Sciences. 2022;12(3):1388.
  40. Evans JD, Lopez DL. Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). Journal of economic entomology. 2004;97(3):752-6.
  41. Shapla UM, Solayman M, Alam N, Khalil MI, Gan SH. 5-Hydroxymethylfurfural (HMF) levels in honey and other food products: effects on bees and human health. Chemistry Central Journal. 2018;12(1):35.
  42. Glatt H, Schneider H, Liu Y. V79-hCYP2E1-hSULT1A1, a cell line for the sensitive detection of genotoxic effects induced by carbohydrate pyrolysis products and other food-borne chemicals. Mutation research/genetic toxicology and environmental mutagenesis. 2005;580(1-2):41-52.
  43. Lee Y-C, Shlyankevich M, Jeong H-K, Douglas JS, Surh Y-J. Bioactivation of 5-hydroxymethyl-2-furaldehyde to an electrophilic and mutagenic allylic sulfuric acid ester. Biochemical and Biophysical Research Communications. 1995;209(3):996-1002.
  44. Monien BH, Engst W, Barknowitz G, Seidel A, Glatt H. Mutagenicity of 5-hydroxymethylfurfural in V79 cells expressing human SULT1A1: identification and mass spectrometric quantification of DNA adducts formed. Chemical research in toxicology. 2012;25(7):1484-92.
  45. Durling LJ, Busk L, Hellman BE. Evaluation of the DNA damaging effect of the heat-induced food toxicant 5-hydroxymethylfurfural (HMF) in various cell lines with different activities of sulfotransferases. Food and Chemical Toxicology. 2009;47(4):880-4.
  46. Mishra V, Shah C, Mokashe N, Chavan R, Yadav H, Prajapati J. Probiotics as potential antioxidants: a systematic review. Journal of agricultural and food chemistry. 2015;63(14):3615-26.
  47. Stecchini ML, Del Torre M, Munari M. Determination of peroxy radical-scavenging of lactic acid bacteria. International journal of food microbiology. 2001;64(1-2):183-8.
  48. Shen Q, Shang N, Li P. In vitro and in vivo antioxidant activity of Bifidobacterium animalis 01 isolated from centenarians. Current microbiology. 2011;62(4):1097-103.
  49. Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, et al. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti–PD-L1 efficacy. Science. 2015;350(6264):1084-9.
  50. Bogdanov S, Jurendic T, Sieber R, Gallmann P. Honey for nutrition and health: a review. Journal of the American college of Nutrition. 2008;27(6):677-89.
  51. Buldini PL, Cavalli S, Mevoli A, Sharma JL. Ion chromatographic and voltammetric determination of heavy and transition metals in honey. Food Chemistry. 2001;73(4):487-95.
  52. Cantarelli MA, Pellerano RG, Marchevsky EJ, Camiña JM. Quality of honey from Argentina: Study of chemical composittion and trace elements. The Journal of Argentine Chemical Society. 2008;96(1-2):33-41.
  53. Conti ME, Finoia MG, Fontana L, Mele G, Botrè F, Iavicoli I. Characterization of Argentine honeys on the basis of their mineral content and some typical quality parameters. Chemistry Central Journal. 2014;8:1-10.
  54. Merin U, Bernstein S, Rosenthal I. A parameter for quality of honey. Food chemistry. 1998;63(2):241-2.
  55. Singh N, Bath PK. Quality evaluation of different types of Indian honey. Food chemistry. 1997;58(1-2):129-33.
  56. Pisani A, Protano G, Riccobono F. Minor and trace elements in different honey types produced in Siena County (Italy). Food Chemistry. 2008;107(4):1553-60.
  57. Gulati OP, Ottaway PB, Jennings S, Coppens P, Gulati N. Botanical nutraceuticals (food supplements and fortified and functional foods) and novel foods in the EU, with a main focus on legislative controls on safety aspects.  Nutraceutical and functional food regulations in the United States and around the World: Elsevier; 2019. p. 277-321.
  58. Ajibola A, Chamunorwa JP, Erlwanger KH. Nutraceutical values of natural honey and its contribution to human health and wealth. Nutrition & metabolism. 2012;9(1):1-12.
  59. Pashte VV, Pashte SV, Said PP. Nutraceutical properties of natural honey to fight health issues: A comprehensive review. Journal of Pharmacognosy and Phytochemistry. 2020;9(5):234-42.