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A MULTIFACETED BIOACTIVITY OF HONEY: INTERACTIONS BETWEEN BEES, PLANTS AND MICROORGANISMS

Year 2024, Volume: 24 Issue: 2, 356 - 385, 18.11.2024
https://doi.org/10.31467/uluaricilik.1511847

Abstract

Honey has been recognized for its medicinal properties for centuries, with well-documented benefits such as antibacterial, anti-inflammatory, and antioxidant activities. However, despite the widespread use of honey for health-related purposes, many of the underlying mechanisms responsible for its bioactivity remain underexplored. This review delves into the complexity of honey’s composition, particularly focusing on the active substances and the honey microbiota contribution to its properties. We aim to bridge the gap in understanding how honey’s multifaceted bioactivity arises from interactions between bees, plants, and microorganisms. The review sheds light on the key compounds, including hydrogen peroxide, methylglyoxal, polyphenols, and antimicrobial peptides, which play vital roles in honey's health benefits. It also highlights the often-overlooked contributions of the honeybee’s gut microbiota and the nectar’s microbiota, which together influence the chemical transformation of nectar into honey and enhance its therapeutic efficacy. By examining the current literature, this article emphasizes the need for deeper investigation into how various factors-such as floral origin, bee subspecies, and environmental conditions-affect the medicinal quality of honey. Understanding these mechanisms could lead to optimized use of honey in medical applications and reveal new therapeutic potentials. This article provides a comprehensive review of the intricate processes and components that make honey not only a nutritional food source but also a potent natural medicine.

Ethical Statement

Ethics committee approval is not required.

Supporting Institution

Russian Science Foundation (RSF)

Project Number

24-16-00179

Thanks

We thanks to Russian Science Foundation (RSF) grant 24-16-00179 for supporting our scientific research in Koltsov Institute of Developmental Biology at 2024.

References

  • Abdulgazina, NM, Farkhutdinov, RG, Yumaguzhin, FG, Veselov, DS. Comparative analysis of phytohormone content in nectar and honey collected by different breeds of bee. Modern Problems of Science and Education. 2015; (2-1): 17749, doi: 10.17513/spno.2015.2.
  • Abee, T, Klaenhammer, TR, Letellier, L. Kinetic studies of the action of lactacin F, a bacteriocin produced by Lactobacillus johnsonii that forms poration complexes in the cytoplasmic membrane. Applied and Environmental Microbiology. 1994; 60(3): 1006-1013, doi: 10.1128/aem.60.3.1006-1013.1994.
  • Abriouel, H, Franz, CMAP, Omar, NB, Gálvez, A. Diversity and applications of Bacillus bacteriocins. FEMS Microbiology Reviews. 2011; 35(1): 201-232, doi: 10.1111/j.1574-6976.2010.00244.x.
  • Alegría, Á, Delgado, S, Roces, C, López, B, Mayo, B. Bacteriocins produced by wild Lactococcus lactis strains isolated from traditional, starter-free cheeses made of raw milk. International Journal of Food Microbiology. 2010; 143(1-2): 61-66, doi: 10.1016/j.ijfoodmicro.2010.07.029.
  • Allison, GE, Worobo, RW, Stiles, ME, Klaenhammer, TR. Heterologous expression of the lactacin F peptides by Carnobacterium piscicola LV17. Applied and Environmental Microbiology. 1995; 61(4): 1371-1377, doi: 10.1128/aem.61.4.1371-1377.1995.
  • Al-Sheraji, SH, Ismail, A, Manap, MY, Mustafa, S, Yusof, RM, Hassan, FA. Prebiotics as functional foods: A review. Journal of Functional Foods. 2013; 5(4): 1542-1553, doi: 10.1016/j.jff.2013.08.009.
  • Alvarez-Pérez, S, Herrera, CM, de Vega, C. Zooming-in on floral nectar: A first exploration of nectar-associated bacteria in wild plant communities. FEMS Microbiology Ecology. 2012; 80(3): 591-602, doi: 10.1111/j.1574-6941.2012.01329.x.
  • Alvarez-Sieiro, P, Montalbán-López, M, Mu, D, Kuipers, OP. Bacteriocins of lactic acid bacteria: Extending the family. Applied Microbiology and Biotechnology. 2016; 100(7): 2939-2951, doi: 10.1007/s00253-016-7343-9.
  • Anderson, KE, Sheehan, TH, Mott, BM, Maes, P, Snyder, L, Schwan, MR, Corby-Harris, V. 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: e83125, doi: 10.1371/journal.pone.0083125.
  • Arredondo, D, Castelli, L, Porrini, MP, Garrido, PM, Eguaras, MJ, Zunino, P, Antunez, K. Lactobacillus kunkeei strains decreased the infection by honey bee pathogens Paenibacillus larvae and Nosema ceranae. Benef Microbes. 2018; 9(2): 279-290, doi: 10.3920/BM2017.0075.
  • Aumeeruddy, MZ, Zengin, G, Mahomoodally, MF. A review of the traditional and modern uses of Salvadora persica L. (Miswak): Toothbrush tree of Prophet Muhammad. Journal of Ethnopharmacology. 2018; 213: 409-444, doi: 10.1016/j.jep.2017.11.030.
  • Bachanova, K, Klaudiny, J, Kopernicky, J, Simuth, J. Identification of honeybee peptide active against Paenibacillus larvae larvae through bacterial growth-inhibition assay on polyacrylamide gel. Apidologie. 2002; 33(3): 259-269, doi: 10.1051/apido:2002015.
  • Balzan, MV, Sadula, R, Scalvenzi, L. Assessing ecosystem services supplied by agroecosystems in Mediterranean Europe: A literature review. Land. 2020; 9(8): 9-24, doi: 10.3390/land9080245.
  • Beretta, G, Caneva, E, Regazzoni, L, Bakhtyari, NG, Maffei Facino, R. A solid-phase extraction procedure coupled to 1H NMR, with chemometric analysis, to seek reliable markers of the botanical origin of honey. Analytica Chimica Acta. 2008; 620(1-2): 176-182, doi: 10.1016/j.aca.2008.05.025.
  • Berríos, P, Fuentes, JA, Salas, D, Carreño, A, Aldea, P, Fernández, F, Trombert, AN. Inhibitory effect of biofilm-forming Lactobacillus kunkeei strains against virulent Pseudomonas aeruginosa in vitro and in honeycomb moth (Galleria mellonella) infection model. Benef Microbes. 2018; 9(2): 257-268, doi: 10.3920/BM2017.0048.
  • Bleau, N, Bouslama, S, Giovenazzo, P, Derome, N. Dynamics of the honeybee (Apis mellifera) gut microbiota throughout the overwintering period in Canada. Microorganisms. 2020; 8(8): 1146, doi: 10.3390/microorganisms8081146.
  • 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): 677-689, doi: 10.1080/07315724.2008.10719745.
  • Bouzo, D, Cokcetin, NN, Li, L, Ballerin, G, Bottomley, AL, Lazenby, J, Whitchurch, CB, Paulsen, IT, Hassan, KA, Harry, EJ. Characterizing the mechanism of action of an ancient antimicrobial, manuka honey, against Pseudomonas aeruginosa using modern transcriptomics. mSystems. 2020; 5(3): e00106-e00120, doi: 10.1128%2FmSystems.00106-20.
  • Bovo, S, Ribani, A, Utzeri, VJ, Schiavo, G, Bertolini, F, Fontanesi, L. Shotgun metagenomics of honey DNA: Evaluation of a methodological approach to describe a multi-kingdom honey bee derived environmental DNA signature. Plos One. 2018; 13(10): e0205575, doi: 10.1371/journal.pone.0205575.
  • Bovo, S, Utzeri, VJ, Ribani, A, Cabbri, R, Fontanesi, L. Shotgun sequencing of honey DNA can describe honey bee derived environmental signatures and the honey bee hologenome complexity. Sci Rep. 2020; 10(1): 9279, doi: 10.1038/s41598-020-66127-1.
  • Brudzynski, K. A current perspective on hydrogen peroxide production in honey. A review. Food Chemistry. 2020; 332: 127229, doi: 10.1016/j.foodchem.2020.127229.
  • Brudzynski, K. Honey as an Ecological Reservoir of Antibacterial Compounds Produced by Antagonistic Microbial Interactions in Plant Nectars, Honey and Honey Bee. Antibiotics (Basel). 2021; 10(5): 551, doi: 10.3390/antibiotics10050551.
  • Brudzynski, K, Abubaker, K, Wang, T. Powerful bacterial killing by buckwheat honeys is concentration-dependent, involves complete DNA degradation and requires hydrogen peroxide. Front. Microbiol. 2012; 3: 242, doi: 10.3389/fmicb.2012.00242.
  • Brudzynski, K, Sjaarda, C. Antibacterial Compounds of Canadian Honeys Target Bacterial Cell Wall Inducing Phenotype Changes, Growth Inhibition and Cell Lysis That Resemble Action of β-Lactam Antibiotics. Plos One. 2014; 9(1): e106967, doi: 10.1371/journal.pone.0106967.
  • Brudzynski, K, Sjaarda, C. Honey Glycoproteins Containing Antimicrobial Peptides, Jelleins of the Major Royal Jelly Protein 1, Are Responsible for the Cell Wall Lytic and Bactericidal Activities of Honey. Plos One. 2015; 10(4): e0120238, doi: 10.1371/journal.pone.0120238.
  • Carter, C, Thornburg, RW. Is the nectar redox cycle a floral defense against microbial attack? Trends in Plant Science. 2004; 9(7): 320-324, doi: 10.1016/j.tplants.2004.05.008.
  • Carter, DA, Blair, SE, Cokcetin, NN, Bouzo, D, Brooks, P, Schothauer, R, Harry, EJ. Therapeutic manuka honey: No longer so alternative. Front Microbiol. 2016; 7: 569, doi: 10.3389/fmicb.2016.00569.
  • Casteels-Josson, K, Zhang, W, Capaci, T, Casteels, P, Tempst, P. Acute transcriptional response of the honey bees peptide-antibiotics gene repertoire, required posttranslational conversion of the precursor structures. Journal of Biological Chemistry. 1994; 269(44): 28569-28575, doi: 10.1016/S0021-9258(19)38548-0.
  • Caulier, S, Nannan, C, Gillis, A, Licciardi, F, Bragard, C, Mahillon, J. Overview of the Antimicrobial Compounds Produced by Members of the Bacillus subtilis Group. Frontiers in Microbiology. 2019; 10: 302, doi: 10.3389/fmicb.2019.00302.
  • Chanclud, E, Lacombe, B. Plant hormones: Key players in gut microbiota and human diseases? Trends in Plant Science. 2017; 22(9): 754-758, doi: 10.1016/j.tplants.2017.07.003.
  • Chauhan, SV, Chorawala, MR. Probiotics, prebiotics, and synbiotics. International Journal of Pharmaceutical Sciences and Research. 2014; 3(12): 711-726, doi: 10.1007/s13197-015-1921-1.
  • Chaven, S. "Chapter 11. Honey, Confectionery and Bakery Products." In "Food Safety Management". Ed. YL-l Motarjemi, H. Academic Press, Cambridge, MA, USA, 2014. p. 283-299. Print.
  • Chick, H, Shin, HS, Ustunol, Z. Growth and acid production by lactic acid bacteria and bifidobacteria grown in skim milk containing honey. Journal of Food Science. 2001; 66(3): 478-481, doi: 10.1111/j.1365-2621. 2001.tb16134.x.
  • Cho, H, Uehara, T, Bernhardt, TG. Beta-lactam antibiotics induce a lethal malfunctioning of the bacterial cell wall synthesis machinery. Cell. 2014; 159(6): 1300-1311, doi: 10.1016/j.cell.2014.11.017.
  • Chua, LS, Lee, JY, Chan, GF. Characterization of the proteins in honey. Analytical Letters. 2014; 48(4): 697-709, doi: 10.1080/00032719.2014.952374.
  • Combarros-Fuertes, P, Fresno, JM, Estevinho, MM, Sousa-Pimenta, M, Tornadijo, ME, Estevinho, LM. Honey: Another Alternative in the Fight against Antibiotic-Resistant Bacteria? Antibiotics (Basel). 2020; 9(11): 774, doi: 10.3390/antibiotics9110774.
  • Conway, PL, Stern, R, Tran, L. The Value-adding Potential of Prebiotic Components of Australian Honey). Rural Industries Research and Development Corporation, Barton, Australia, 2010, p. 30.
  • Corby-Harris, V, Maes, P, Anderson, KE. The bacterial communities associated with honey bee (Apis mellifera) foragers. Plos One. 2014; 9(4): e95056, doi: 10.1371/journal.pone.0095056.
  • da Silva, PM, Gauche, C, Gonzaga, LV, Costa, AC, Fett, R. Honey: Chemical composition, stability and authenticity. Food Chemistry. 2016; 196: 309-323, doi: 10.1016/j.foodchem.2015.09.051.
  • David, LA, Maurice, CF, Carmody, RN, Gootenberg, DB, Button, JE, Wolfe, BE, Ling, AV, Devlin, AS, Varma, Y, Fischbach, MA, Biddinger, SB, Dutton, RJ, Turnbaugh, PJ. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014; 505(7484): 559-563, doi: 10.1038/nature12820.
  • de Melo, FHC, Menezes, FNDD, de Sousa, JMB, dos Santos Lima, M, da Silva Campelo Borges, G, de Souza, EL, Magnani, M, International, FR. Prebiotic activity of monofloral honeys produced by stingless bees in the semi-arid region of Brazilian northeastern toward Lactobacillus acidophilus LA-05 and Bifidobacterium lactis BB-12. Food Research International. 2020; 128: 108809, doi: 10.1016/j.foodres.2019.108809.
  • De Vuyst, L, Leroy, F. Bacteriocins from lactic acid bacteria: Production, purification, and food applications. Journal of Molecular Microbiology and Biotechnology. 2007; 13(4): 194-199, doi: 10.1159/000104752.
  • Deleu, M, Lorent, J, Lins, L, Brasseur, R, Braun, N, El Kirat, K, Nylander, T, Dufrêne, YF, Mingeot-Leclercq, MP. Effects of surfactin on membrane models displaying lipid phase separation. Biochimica et Biophysica Acta. 2013; 1828(2): 801-815, doi: 10.1016/j.bbamem.2012.11.007.
  • Deshmukh, SK, Verekar, SA, Bhave, SV. Endophytic fungi: A reservoir of antibacterials. Frontiers in Microbiology. 2015; 5: 715, doi: 10.3389/fmicb.2014.00715.
  • Di Girolamo, F, D'Amato, A, Righetti, PG. Assessment of the floral origin of honey via proteomic instruments. Journal of Proteomics. 2012; 75(12): 3688-3693, doi: 10.1016/j.jprot.2012.04.029.
  • Disayathanoowat, T, Li, H, Supapimon, N, Suwannarach, N, Lumyong, S, Chantawannakul, P, Guo, J. Different dynamics of bacterial and fungal communities in hive-stored bee bread and their possible roles: A case study from two commercial honey bees in China. Microorganisms. 2020; 8(2): 264, doi: 10.3390/microorganisms8020264.
  • Dong, ZX, Li, HY, Chen, YF, Wang, F, Deng, XY, Lin, LB, Zhang, QL, Li, J, Guo, J. Colonization of the gut microbiota of honey bee (Apis mellifera) workers at different developmental stages. Microbiol Res. 2020; 231: 126370, doi: 10.1016/j.micres.2019.126370.
  • Elzeini, HM, Ali, A, Nasr, NF, Hassan, M, Hassan, AAM, Elenany, YE. Probiotic capability of novel lactic acid bacteria isolated from worker honey bees gut microbiota. FEMS Microbiology Letters. 2021; 368(6): fnab030, doi: 10.1093/femsle/fnab030.
  • Endo, A, Salminen, S. Honeybees and beehives are rich sources for fructophilic lactic acid bacteria. Systematic and Applied Microbiology. 2013; 36(6): 444-448, doi: 10.1016/j.syapm.2013.05.011.
  • Erban, T, Shcherbachenko, E, Talacko, P, Harant, K. The Unique Protein Composition of Honey Revealed by Comprehensive Proteomic Analysis: Allergens, Venom-like Proteins, Antibacterial Properties, Royal Jelly Proteins, Serine Proteases, and Their Inhibitors. Journal of Natural Products. 2019; 82(5): 1217-1226, doi: 10.1021/acs.jnatprod.8b01061.
  • Evans, JD, Aronstein, K, Chen, YP, Hetru, C, Imler, JL, Jiang, H, Kanost, M, Thompson, GJ, Zou, Z, Hultmark, D. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Molecular Biology. 2006; 15(5): 645-656, doi: 10.1111/j.1365-2583.2006.00682.x.
  • Forsgren, E, Olofsson, TC, Vásquez, A, Fries, I. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie. 2009; 41(1): 99-108, doi: 10.1051/apido/2009065.
  • Fuandila, NN, Widanarni, W, Yuhana, M. Growth performance and immune response of prebiotic honey fed Pacific white shrimp Litopenaeus vannamei to Vibrio parahaemolyticus infection. Journal of Applied Aquaculture. 2019; 32(3): 221-235, doi: 10.1080/10454438.2019.1615593.
  • Fujiwara, S, Imai, J, Fujiwara, M, Yaeshima, T, Kawashima, T, Kobayashi, K. A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. Journal of Biological Chemistry. 1990; 265(19): 11333-11337, doi: 10.1016/S0021-9258(19)38596-5.
  • Genersch, E. American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. Journal of Invertebrate Pathology. 2010; 103: S10-S19, doi: 10.1016/j.jip.2009.06.015.
  • Gibson, GR, Roberfroid, MB. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. Journal of Nutrition. 1995; 125(6): 1401-1412, doi: 10.1093/jn/125.6.1401.
  • Gong, HS, Meng, XC, Wang, H. Mode of action of plantaricin MG, a bacteriocin active against Salmonella typhimurium. Journal of Basic Microbiology. 2010; 50(1): S37-S45, doi: 10.1002/jobm.200900307.
  • Gou, W, Fu, Y, Yue, L, Chen, G-d, Cai, X, Shuai, M, Xu, F, Yi, X, Chen, H, Zhu, Y, Xiao, M-l, Jiang, Z, Miao, Z, Xiao, C, Shen, B, Wu, X, Zhao, H, Ling, W, Wang, J, Chen, Y-m, Guo, T, Zheng, J-S. Gut microbiota may underlie the predisposition of healthy individuals to COVID-19. Research square. 2020; 1: 1-24, doi: 10.21203/rs.3.rs-45991/v1.
  • Grady, EN, MacDonald, J, Liu, L, Richman, A, Yuan, ZC. Current knowledge and perspectives of Paenibacillus: A review. Microb Cell Fact. 2016; 15(1): 203, doi: 10.1186/s12934-016-0603-7.
  • Haddadin, MSY, Jamal Abu, INS, Robinson, RK. Effect of honey on the growth and metabolism of two bacterial species of intestinal origin. Pakistan Journal of Nutrition. 2007; 6(6): 693-697, doi: 10.3923/pjn.2007.693.697.
  • Hamayun, M, Hussain, A, Khan, SA, Kim, HY, Khan, AL, Waqas, M, Irshad, M, Iqbal, A, Rehman, G, Jan, S, Lee, IJ. Gibberellins producing endophytic fungus Porostereum spadiceum AGH786 rescues growth of salt-affected soybean. Front Microbiol. 2017; 8: 686, doi: 10.3389/fmicb.2017.00686.
  • Hammond, EN, Donkor, ES. Antibacterial effect of manuka honey on Clostridium difficile. BMC Research Notes. 2013; 6: 188, doi: 10.1186/1756-0500-6-188.
  • Hasyimi, W, Widanarni, W, Yuhana, M. Growth performance and intestinal microbiota diversity in Pacific white shrimp Litopenaeus vannamei fed with a probiotic bacterium, honey prebiotic, and synbiotic. Current Microbiology. 2020; 77(10): 2982-2990, doi: 10.1007/s00284-020-02117-w.
  • Henriques, AF, Jenkins, RE, Burton, NF, Cooper, RA. The effect of manuka honey on the structure of Pseudomonas aeruginosa. European Journal of Clinical Microbiology & Infectious Diseases. 2011; 30(2): 167-171, doi: 10.1007/s10096-010-1073-y.
  • Herold, E, Leibold, G. Heilwerte aus dem Bienenvolk). Kosmos (Franckh-Kosmos), Germany, 2000, p.
  • Hiel, S, Bindels, LB, Pachikian, BD, Kalala, G, Broers, V, Zamariola, G, Chang, BPI, Kambashi, B, Rodriguez, J, Cani, PD, Neyrinck, AM, Thissen, JP, Luminet, O, Bindelle, J, Delzenne, NM. Effects of a diet based on inulin-rich vegetables on gut health and nutritional behavior in healthy humans. American Journal of Clinical Nutrition. 2019; 109(6): 1683-1695, doi: 10.1093/ajcn/nqz001.
  • Hilgarth, M, Redwitz, J, Ehrmann, MA, Vogel, RF, Jakob, F. Bombella favorum sp. Nov. And Bombella mellum sp. Nov., two novel species isolated from the honeycombs of Apis mellifera. Int J Syst Evol Microbiol. 2021; 71(2): 10.1099/ijsem.1090.004633, doi: 10.1099/ijsem.0.004633.
  • Ilyasov, RA, Nikolenko, AG, Saifullina, N. Dark forest bee Apis mellifera mellifera L. of the Republic of Bashkortostan). Gilem, Bashkortostan Encyclical, Ufa, Russia, 2015, p. 308.
  • Isah, T. Stress and defense responses in plant secondary metabolites production. Biol. Res. 2019; 52(1): 39, doi: 10.1186/s40659-019-0264-y.
  • Jack, RW, Tagg, JR, Ray, B. Bacteriocins of Gram-positive bacteria. Microbiological Reviews. 1995; 59(2): 171, doi: 10.1128/mr.59.2.171-200.1995.
  • Janek, T, Drzymała, K, Dobrowolski, A. In vitro efficacy of the lipopeptide biosurfactant surfactin-C15 and its complexes with divalent counterions to inhibit Candida albicans biofilm and hyphal formation. Bio-fouling. 2020; 36: 210-221, doi: 10.1080/08927014.2020.1720453.
  • Jiang, L, Xie, M, Chen, G, Qiao, J, Zhang, H, Zeng, X. Phenolics and carbohydrates in buckwheat honey regulate the human intestinal microbiota. JF. Ecology and Evolution. 2020; 8: 6432942, doi: 10.1155/2020/6432942.
  • Johnston, M, McBride, M, Dahiya, D, Owusu-Apenten, R, Nigam, PS. Antibacterial activity of Manuka honey and its components: An overview. AIMS microbiology. 2018; 4(4): 655-664, doi: 10.3934/microbiol.2018.4.655.
  • Jones, JC, Fruciano, C, Hildebrand, F, Al Toufalilia, H, Balfour, NJ, Bork, P, Engel, P, Ratnieks, FLW, Hughes, WOH. Gut microbiota composition is associated with environmental landscape in honey bees. Ecology and Evolution. 2017; 8(1): 441-451, doi: 10.1002/ece3.3597.
  • Kačániová, M, Pavlicova, S, Hascik, P, Kociubinski, G, Knazovicka, V, Sudzina, M, Sudzinova, J, Fikselova, M. Microbial communities in bees, pollen and honey from Slovakia. Acta Microbiologica et Immunologica Hungarica. 2009; 56(3): 285-295, doi: 10.1556/AMicr.56.2009.3.7.
  • Kafantaris, I, Amoutzias, GD, Mossialos, D. Foodomics in bee product research: A systematic literature review. European Food Research and Technology. 2020; 247(2): 309-331, doi: 10.1007/s00217-020-03634-5.
  • Karabagias, IK. A targeted metabolomic procedure for the identification of isophorone-related compounds in honey. Journal of Plant Biochemistry & Physiology. 2018; 6(01): 10.4172/2329-9029.1000210, doi: 10.4172/2329-9029.1000210.
  • Keller, A, Brandel, A, Becker, MC, Balles, R, Abdelmohsen, UR, Ankenbrand, MJ, Sickel, W. Wild bees and their nests host Paenibacillus bacteria with functional potential of avail. Microbiome. 2018; 6(1): 229, doi: 10.1186/s40168-018-0614-1.
  • Kešnerová, L, Emery, O, Troilo, M, Liberti, J, Erkosar, B, Engel, P. Gut microbiota structure differs between honeybees in winter and summer. ISME J. 2020; 14(3): 801-814, doi: 10.1038/s41396-019-0568-8.
  • 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): 414-421, doi: 10.1099/ijsem.0.000736.
  • Khalil, MI, Alam, N, Moniruzzaman, M, Sulaiman, SA, Gan, SH. Phenolic acid composition and antioxidant properties of Malaysian honeys. Journal of Food Science. 2011; 76(6): C921-928, doi: 10.1111/j.1750-3841.2011.02282.x.
  • Khan, A, Doshi, HV, Thakur, MC. "Bacillus spp.: A Prolific Siderophore Producer." In "Bacilli and Agrobiotechnology". Ed. MR Islam, M. Pandey, P. Jha, C. Aeron, A. Springer, Cham, Switzerland, 2016. p. 255. Print.
  • Klaudiny, J, Albert, S, Bachanová, K, Kopernický, J, Šimúth, J. Two structurally different defensin genes, one of them encoding a novel defensin isoform, are expressed in honeybee Apis mellifera. Insect Biochemistry and Molecular Biology. 2005; 35(1): 11-22, doi: 10.1016/j.ibmb.2004.09.007.
  • Kňazovická, V. Diversity of Bacteria in Slovak and Foreign Honey, with Assessment of Its Physico-Chemical Quality and Counts of Cultivable Microorganisms. Journal of Microbiology, Biotechnology and Food Sciences. 2019; 9(Special issue): 414-421, doi: 10.15414/jmbfs.2019.9.special.414-421.
  • Kolayli, S, Boukraâ, L, Sahin, H, Abdellah, F. "Sugars in honey." In "Dietary sugars: chemistry, analysis, function and effects". Ed. VR Preedy. The Royal Society of Chemistry, Cambridge, UK, 2012. p. 3-15. Print.
  • Kurek-Gorecka, A, Gorecki, M, Rzepecka-Stojko, A, Balwierz, R, Stojko, J. Bee products in dermatology and skin care. Molecules. 2020; 25(3): 10.3390/molecules25030556, doi: 10.3390/molecules25030556.
  • Kwakman, PH, te Velde, AA, de Boer, L, Speijer, D, Vandenbroucke-Grauls, CM, Zaat, SA. How honey kills bacteria. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2010; 24(7): 2576-2582, doi: 10.1096/fj.09-150789.
  • Lebedev, VI, Murashova, EA. Influence of breed and placement of brood on the quality of honey. Russian Journal of Beekeeping " Pchelovodstvo". 2004; (3): 50-52, doi:
  • Lee, H, Churey, JJ, Worobo, RW. Purification and structural characterization of bacillomycin F produced by a bacterial honey isolate active against Byssochlamys fulva H25. Journal of Applied Microbiology. 2008; 105(3): 663-673, doi: 10.1111/j.1365-2672.2008.03797.x.
  • Lee, H, Churey, JJ, Worobo, RW. Biosynthesis and transcriptional analysis of thurincin H, a tandem repeated bacteriocin genetic locus, produced by Bacillus thuringiensis SF361. FEMS Microbiology Letters. 2009; 299(2): 205-213, doi: 10.1111/j.1574-6968.2009.01749.x.
  • Lee, JH, Park, JH, Kim, JA, Neupane, GP, Cho, MH, Lee, CS, Lee, J. Low concentrations of honey reduce biofilm formation, quorum sensing, and virulence in Escherichia coli O157:H7. Biofouling. 2011; 27(10): 1095-1104, doi: 10.1080/08927014.2011.633704.
  • Leeming, ER, Johnson, AJ, Spector, TD, Le Roy, CI. Effect of Diet on the Gut Microbiota: Rethinking Intervention Duration. Nutrients. 2019; 11(12): 2862, doi: 10.3390/nu11122862.
  • Li, Y, Long, S, Liu, Q, Ma, H, Li, J, Xiaoqing, W, Yuan, J, Li, M, Hou, B. Gut microbiota is involved in the alleviation of loperamide-induced constipation by honey supplementation in mice. Food Sci Nutr. 2020; 8(8): 4388-4398, doi: 10.1002/fsn3.1736.
  • Liu, GL, Chi, Z, Wang, GY, Wang, ZP, Li, Y, Chi, ZM. Yeast killer toxins, molecular mechanisms of their action and their applications. Critical Reviews in Biotechnology. 2015; 35: 222–234, doi: 10.3109/07388551.2013.879318.
  • Luong, DV, Tam, NQ, Xuan, DTT, Tai, NT. NMR based metabolomic approach for evaluation of Vietnamese honey. Vietnam Journal of Chemistry. 2019; 57(6): 712-716, doi: 10.1002/vjch.2019000101.
  • Machado De-Melo, A, De Almeida-Muradian, L, Sancho, M, Pascual Maté, A. Composition and properties of Apis mellifera honey: A review. Journal of Apicultural Research. 2017; 57(1): 1-33, doi: 10.1080/00218839.2017.1338444.
  • Maddocks, SE, Jenkins, RE. Honey: A sweet solution to the growing problem of antimicrobial resistance? Future Microbiology. 2013; 8(11): 1419-1429, doi: 10.2217/fmb.13.105.
  • Martinson, VG, Moy, J, Moran, NA. Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol. 2012; 78(8): 2830-2840, doi: 10.1128/AEM.07810-11.
  • 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. Mol. Nutr. Food Res. 2008; 52(4): 483-489, doi: 10.1002/mnfr.200700282.
  • McAuliffe, OR, Ross, P, Hill, C. Lantibiotics: Structure, biosynthesis and mode of action. FEMS Microbiology Reviews. 2001; 25(3): 285-308, doi: 10.1111/j.1574-6976.2001.tb00579.x.
  • Meng, F, Liu, Y, Nie, T, Tang, C, Lyu, F, Bie, X, Lu, Y, Zhao, M, Lu, Z. Plantaricin A, Derived from Lactiplantibacillus plantarum, Reduces the Intrinsic Resistance of Gram-Negative Bacteria to Hydrophobic Antibiotics. Applied and Environmental Microbiology. 2022; 88(10): e0037122, doi: 10.1128/aem.00371-22.
  • Miethke, M, Klotz, O, Linne, U, May, JJ, Beckering, CL, Marahiel, MA. Ferri-bacillibactin uptake and hydrolysis in Bacillus subtilis. Molecular Microbiology. 2006; 61(6): 1413-1427, doi: 10.1111/j.1365-2958.2006.05321.x.
  • Miguel, MG, Antunes, MD, Faleiro, ML. Honey as a complementary medicine. Integrative Medicine Insights. 2017; 12: 1178633717702869, doi: 10.1177/1178633717702869.
  • Mohan, A, Quek, S-Y, Gutierrez-Maddox, N, Gao, Y, Shu, Q. Effect of honey in improving the gut microbial balance. Food Quality and Safety. 2017; 1(2): 107-115, doi: 10.1093/fqsafe/fyx015.
  • Muhialdin, BJ, Hassan, Z, Saari, N. In vitro antifungal activity of lactic acid bacteria low molecular peptides against spoilage fungi of bakery products. Annals of Microbiology. 2018; 68(8): 557-567, doi: 10.1007/s13213-018-1332-8.
  • Mukherjee, A, Gaurav, AK, Singh, S, Yadav, S, Bhowmick, S, Abeysinghe, S, Verma, JP. The bio-active potential of phytohormones: A review. Biotechnology Reports. 2022; 35: e00748, doi: 10.1016/j.btre.2022.e00748.
  • Nagpal, R, Kaur, A. Synbiotic effect of various prebiotics on in vitro activities of probiotic Lactobacilli. Ecology of Food and Nutrition. 2011; 50(1): 63-68, doi: 10.1080/03670244.2011.539161.
  • Naseer, S, Khan, S, Azim, K. Identification of cultivable bacteria from natural honey of different botanical origin. Pakistan Journal of Biochemistry and Molecular Biology. 2015; 48: 53-56, doi:
  • Nolan, VC, Harrison, J, Cox, JAG. Dissecting the Antimicrobial Composition of Honey. Antibiotics (Basel). 2019; 8(1): 251, doi: 10.3390/antibiotics8040251.
  • Nooh, HZ, Nour-Eldien, NM. The anti dual-inflammatory and antioxidant activities of natural honey promote cell proliferation and neural regeneration in a rat model of colitis. Acta Histochem. 2016; 118(6): 588-595, doi: 10.1016/j.acthis.2016.06.006.
  • Nowak, A, Szczuka, D, Gorczynska, A, Motyl, I, Kregiel, D. Characterization of Apis mellifera gastrointestinal microbiota and lactic acid bacteria for honeybee protection—a review. Cells. 2021; 10(3): 701, doi: 10.3390/cells10030701.
  • Olaitan, PB, Adeleke, OE, Ola, IO. Honey: A reservoir for microorganisms and an inhibitory agent for microbes. African Health Sciences. 2007; 7(3): 159-165, doi: 10.5555/afhs.2007.7.3.159.
  • Olawode, EO, Tandlich, R, Cambray, G. (1)H-NMR Profiling and Chemometric Analysis of Selected Honeys from South Africa, Zambia, and Slovakia. Molecules. 2018; 23(3)doi: 10.3390/molecules23030578.
  • Olofsson, TC, Alsterfjord, M, Nilson, B, Butler, E, Vázquez, 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(Pt 9): 3109-3119, doi: 10.1099/ijs.0.059600-0.
  • Olofsson, TC, Butler, E, Markowicz, P, Lindholm, C, Larsson, L, Vázquez, A. Lactic bacterial acid symbionts in honeybees - an unknown key to honey's antimicrobial and therapeutic activities. International Wound Journal. 2016; 13(5): 668-679, doi: 10.1111/iwj.12345.
  • Olofsson, TC, Vasquez, 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): 356-363, doi: 10.1007/s00284-008-9202-0.
  • Oscáriz, JC, Pisabarro, AG. Classification and mode of action of membrane-active bacteriocins produced by gram-positive bacteria. International Microbiology. 2001; 4(1): 13-19, doi: 10.1007/s10123-001-0056-y.
  • Pajor, M, Worobo, RW, Milewski, S, Szweda, P. The Antimicrobial Potential of Bacteria Isolated from Honey Samples Produced in the Apiaries Located in Pomeranian Voivodeship in Northern Poland. International Journal of Environmental Research and Public Health. 2018; 15(9)doi: 10.3390/ijerph15092002.
  • Pajor, M, Xiong, ZR, Worobo, RW, Szweda, P. Paenibacillus alvei MP1 as a Producer of the Proteinaceous Compound with Activity against Important Human Pathogens, Including Staphylococcus aureus and Listeria monocytogenes. Pathogens. 2020; 9(4): 319, doi: 10.3390/pathogens9040319.
  • Parada, JL, Caron, CR, Medeiros, ABP, Soccol, CR. Bacteriocins from lactic acid bacteria: Purification, properties and use as biopreservatives. Brazilian Archives of Biology and Technology. 2007; 50(4): 521–542, doi: 10.1590/S1516-89132007000300018
  • Paraszkiewicz, K, Moryl, M, Płaza, G, Bhagat, D, Satpute, SK, Bernat, P. Surfactants of microbial origin as antibiofilm agents. International Journal of Environmental Health Research. 2019; 31: 401-420, doi: 10.1080/09603123.2019.1579732.
  • Poirel, L, Jayol, A, Nordmann, P. Polymyxins: Antibacterial Activity, Susceptibility Testing, and Resistance Mechanisms Encoded by Plasmids or Chromosomes. Clinical Microbiology Reviews. 2017; 30(2): 557-596, doi: 10.1128/CMR.00064-16.
  • Pomastowski, P, Zloch, M, Rodzik, A, Ligor, M, Kostrzewa, M, Buszewski, B. Analysis of bacteria associated with honeys of different geographical and botanical origin using two different identification approaches: MALDI-TOF MS and 16S rDNA PCR technique. Plos One. 2019; 14(5): e0217078, doi: 10.1371/journal.pone.0217078.
  • Popa, D, Ustunol, Z. Influence of sucrose, high fructose corn syrup and honey from different floral sources on growth and acid production by lactic acid bacteria and bifidobacteria. International Journal of Dairy Technology. 2011; 64(2): 247-253, doi: 10.1111/j.1471-0307.2011.00666.x.
  • 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(4): 1248-1260, doi: 10.1111/jam.14469.
  • Ranneh, Y, Akim, AM, Hamid, HA, Khazaai, H, Fadel, A, Zakaria, ZA, Albujja, M, Bakar, MFA. Honey and its nutritional and anti-inflammatory value. BMC Complement Med Ther. 2021; 21(1): 30, doi: 10.1186/s12906-020-03170-5.
  • Raschka, L, Daniel, H. Mechanisms underlying the effects of inulin-type fructans on calcium absorption in the large intestine of rats. Bone. 2005; 37(5): 728-735, doi: 10.1016/j.bone.2005.05.015.
  • Raymann, K, Bobay, LM, Moran, NA. Antibiotics reduce genetic diversity of core species in the honeybee gut microbiome. Molecular Ecology. 2018; 27(8): 2057-2066, doi: 10.1111/mec.14434.
  • Raymann, K, Shaffer, Z, Moran, NA. Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biology. 2017; 15(3): e2001861, doi: 10.1371/journal.pbio.2001861.
  • Rea, MC, Sit, CS, Clayton, E, O’Connor, PM, Whittal, RM, Zheng, J, Vederas, JC, Ross, RP, Hill, C, Rutherford, ST, Bassler, BL. Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile Bacterial quorum sensing: Its role in virulence and possibilities for its control. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(20): 9352-9357, doi: 10.1073/pnas.0913554107.
  • Roberfroid, M, Gibson, GR, Hoyles, L, McCartney, AL, Rastall, R, Rowland, I, Wolvers, D, Watzl, B, Szajewska, H, Stahl, B, Guarner, F, Respondek, F, Whelan, K, Coxam, V, Davicco, MJ, Leotoing, L, Wittrant, Y, Delzenne, NM, Cani, PD, Neyrinck, AM, Meheust, A. Prebiotic effects: Metabolic and health benefits. British Journal of Nutrition. 2010; 104 Suppl 2: S1-S63, doi: 10.1017/S0007114510003363.
  • Rodríguez-Andrade, E, Stchigel, AM, Terrab, AJ, Guarro, A, Cano-Lira, JF. Diversity of xerotolerant and xerophilic fungi in honey. IMA Fungus. 2019; 10(1): 20, doi: 10.1186/s43008-019-0017-6.
  • Rosendale, DI, Maddox, IS, Miles, MC, Rodier, M, Skinner, M, Sutherland, J. High-throughput microbial bioassays to screen potential New Zealand functional food ingredients intended to manage the growth of probiotic and pathogenic gut bacteria. International Journal of Food Science & Technology. 2008; 43(12): 2257-2267, doi: 10.1111/j.1365-2621.2008.01863.x.
  • Rutherford, ST, Bassler, BL. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harbor Perspectives in Medicine. 2012; 2(11)doi: 10.1101/cshperspect.a012427.
  • Sadiq, FA, Yan, B, Tian, F, Zhao, J, Zhang, H, Chen, W. Lactic Acid Bacteria as Antifungal and Anti-Mycotoxigenic Agents: A Comprehensive Review. Comprehensive Reviews in Food Science and Food Safety. 2019; 18(5): 1403-1436, doi: 10.1111/1541-4337.12471.
  • Samaranayaka, AGP, Li-Chan, ECY. Food-derived peptidic antioxidants: A review of their production, assessment, and potential applications. Journal of Functional Foods. 2011; 3(4): 229-254, doi: 10.1016/j.jff.2011.05.006.
  • Sanz, ML, González, M, de Lorenzo, C, Sanz, J, Martínez-Castro, I. Carbohydrate composition and physicochemical properties of artisanal honeys from Madrid (Spain): Occurrence of Echium sp honey. Journal of the Science of Food and Agriculture. 2004; 84(12): 1577-1584, doi: 10.1002/jsfa.1823.
  • Sanz, ML, Polemis, N, Morales, V, Corzo, N, Drakoularakou, A, Gibson, GR, Rastall, RA. In vitro investigation into the potential prebiotic activity of honey oligosaccharides. Journal of Agricultural and Food Chemistry. 2005; 53(8): 2914-2921, doi: 10.1021/jf0500684.
  • Scarfi, S, Ferraris, C, Fruscione, F, Fresia, C, Guida, L, Bruzzone, S, Usai, C, Parodi, A, Millo, E, Salis, A, Burastero, G, De Flora, A, Zocchi, E. Cyclic ADP ribose-mediated expansion and stimulation of human mesenchymal stem cells by the plant hormone abscisic acid. Stem Cells. 2008; 26(11): 2855-2864, doi: 10.1634/stemcells.2008-0488.
  • Schell, KR, Fernandes, KE, Shanahan, E, Wilson, I, Blair, SE, Carter, DA, Cokcetin, NN. The potential of honey as a prebiotic food to re-engineer the gut microbiome toward a healthy state. Frontiers in Nutrition. 2022; 9: 957932, doi: 10.3389/fnut.2022.957932.
  • Schramm, DD, Karim, M, Schrader, HR, Holt, RR, Cardetti, M, Keen, CL. Honey with high levels of antioxidants can provide protection to healthy human subjects. Journal of Agricultural and Food Chemistry. 2003; 51(6): 1732-1735, doi: 10.1021/jf025928k.
  • Seraglio, SKT, Silva, B, Bergamo, G, Brugnerotto, P, Gonzaga, LV, Fett, R, Costa, ACO. An overview of physicochemical characteristics and health-promoting properties of honeydew honey. Food Research International. 2019; 119: 44-66, doi: 10.1016/j.foodres.2019.01.028.
  • Sharma, D, Saharan, BS. Functional characterization of biomedical potential of biosurfactant produced by Lactobacillus helveticus. Biotechnology Reports. 2016; 11: 27-35, doi: 10.1016/j.btre.2016.08.005.
  • Shin, HS, Ustunol, Z. Carbohydrate composition of honey from different floral sources and their influence on the growth of selected intestinal bacteria: An in vitro comparison. Food Research International. 2005; 38(6): 721-728, doi: 10.1016/j.foodres.2005.01.007.
  • Sinacori, M, Francesca, N, Alfonzo, A, Cruciata, M, Sannino, C, Settanni, L, Moschetti, G. Cultivable microorganisms associated with honeys of different geographical and botanical origin. Food Microbiology. 2014; 38: 284-294, doi: 10.1016/j.fm.2013.07.013.
  • Slačanac, V, Lučan, M, Hardi, J, Krstanović, V, Koceva Komlenić, D. Fermentation of honey-sweetened soymilk with Bifidobacterium lactis Bb-12 and Bifidobacterium longum Bb-46: fermentation activity of bifidobacteria and in vitro antagonistic effect against Listeria monocytogenes FSL N1-017. Czech Journal of Food Sciences. 2012; 30(4): 321-329, doi: 10.17221/190/2011-CJFS.
  • Snowdon, JA, Cliver, DO. Microorganisms in honey. International Journal of Food Microbiology. 1996; 31(1-3): 1-26, doi: 10.1016/0168-1605(96)00970-1.
  • Sood, S, Steinmetz, H, Beims, H, Mohr, KI, Stadler, M, Djukic, M, von der Ohe, W, Steinert, M, Daniel, R, Müller, R. Paenilarvins: Iturin family lipopeptides from the honey bee pathogen Paenibacillus larvae. ChemBioChem. 2014; 15(13): 1947-1955, doi: 10.1002/cbic.201402139.
  • Straight, PD, Fischbach, MA, Walsh, CT, Rudner, DZ, Kolter, R. A singular enzymatic mega-complex from Bacillus subtilis. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104: 305-310, doi: 10.1073/pnas.0609073104.
  • Sudisha, J, Sharathchandra, RG, Amruthesh, KN, Kumar, A, Shetty, HS. "Pathogenesis Related Proteins in Plant Defense Response." In "Plant Defence: Biological Control. Progress in Biological Control". 2011. p. 12. Print.
  • Sumi, CD, Yang, BW, Yeo, IC, Hahm, YT. Antimicrobial peptides of the genus Bacillus: A new era for antibiotics. Canadian Journal of Microbiology. 2015; 61(2): 93-103, doi: 10.1139/cjm-2014-0613.
  • Tanes, C, Bittinger, K, Gao, Y, Friedman, ES, Nessel, L, Paladhi, UR, Chau, L, Panfen, E, Fischbach, MA, Braun, J, Xavier, RJ, Clish, CB, Li, H, Bushman, FD, Lewis, JD, Wu, GD. Role of dietary fiber in the recovery of the human gut microbiome and its metabolome. Cell Host Microbe. 2021; 29(3): 394-407, doi: 10.1016/j.chom.2020.12.012.
  • Tiihonen, K, Ouwehand, AC, Rautonen, N. Human intestinal microbiota and healthy ageing. Ageing Res Rev. 2010; 9(2): 107-116, doi: 10.1016/j.arr.2009.10.004.
  • Tola, YH, Waweru, JW, Hurst, GDD, Slippers, B, Paredes, JC. Characterization of the Kenyan honey bee (Apis mellifera) gut microbiota: A first look at tropical and sub-Saharan African bee-associated microbiomes. Microorganisms. 2020; 8(11): 1721, doi: 10.3390/microorganisms8111721.
  • Turski, MP, Turska, M, Zgrajka, W, Kuc, D, Turski, WA. Presence of kynurenic acid in food and honeybee products. Amino Acids. 2009; 36(1): 75-78, doi: 10.1007/s00726-008-0031-z.
  • Upreti, GC, Hinsdill, RD. Production and mode of action of lactocin 27: Bacteriocin from a homofermentative Lactobacillus. Antimicrobial Agents and Chemotherapy. 1975; 7(2): 139-145, doi: 10.1128/aac.7.2.139.
  • Vakhonina, TV. Bee pharmacy). Institute of Beekeeping, Rybnoye, Russia, 2002, p. 190.
  • Vallianou, NG. Honey and its anti-inflammatory, anti-bacterial, and anti-oxidant properties. General Medicine. 2014; 02(02): 132, doi: 10.4172/2327-5146.1000132.
  • Vásquez, A, Forsgren, E, Fries, I, Paxton, RJ, Flaberg, E, Szekely, L, Olofsson, TC. Symbionts as major modulators of insect health: Lactic acid bacteria and honeybees. Plos One. 2012; 7(3): e33188, doi: 10.1371/journal.pone.0033188.
  • Vásquez, A, Olofsson, TC. The lactic acid bacteria involved in the production of bee pollen and bee bread. Journal of Apicultural Research. 2009; 48(3): 189-195, doi: 10.3896/Ibra.1.48.3.07.
  • Venkatesh, N, Keller, NP. Mycotoxins in Conversation with Bacteria and Fungi. Frontiers in Microbiology. 2019; 10: 403, doi: 10.3389/fmicb.2019.00403.
  • Vlamakis, H, Chai, Y, Beauregard, P, Losick, R, Kolter, R. Sticking together: Building a biofilm the Bacillus subtilis way. Nature Reviews Microbiology. 2013; 11(3): 157-168, doi: 10.1038/nrmicro2960.
  • Voller, J, Maková, B, Kadlecová, A, Gonzalez, G, Strnad, M. "Plant hormone cytokinins for modulating human aging and age-related diseases." In "Hormones in Ageing and Longevity". Ed. SS Rattan, Ramesh. Springer Cham, Cham, Germany, 2017. p. 311-335. Print.
  • Vrabie, V, Yazlovitska, L, Ciochină, V, Rotaru, S. Comparative content of free amino acids in pollen and honey. Bulletin Ştiinţific. Revista de Etnografie, Ştiinţele Naturii şi Muzeologie (Serie Nouă). 2019; 30(43): 71-78, doi:
  • Wang, K, Li, J, Zhao, L, Mu, X, Wang, C, Wang, M, Wu, L. Gut microbiota protects honey bees (Apis mellifera L.) against polystyrene microplastics exposure risks. Journal of Hazardous Materials. 2021; 402: 123828, doi: 10.1016/j.jhazmat.2020.123828.
  • Wang, K, Wan, ZR, Ou, AQ, Liang, XW, Guo, XX, Zhang, ZY, Xue, XF. Monofloral honey from a medical plant, Prunella vulgaris, protected against dextran sulfate sodium-induced ulcerative colitis via modulating gut microbial populations in rats. Food & Function. 2019; 10(7): 3828-3838, doi: 10.1039/c9fo00460b.
  • Wang, Q, Cai, WJ, Yu, L, Ding, J, Feng, YQ. Comprehensive profiling of phytohormones in honey by sequential liquid-liquid extraction coupled with liquid chromatography-mass spectrometry. Journal of Agricultural and Food Chemistry. 2017; 65(3): 575-585, doi: 10.1021/acs.jafc.6b04234.
  • Wen, Y, Wang, L, Jin, Y, Zhang, J, Su, L, Zhang, X, Zhou, J, Li, Y. The Microbial Community Dynamics during the Vitex Honey Ripening Process in the Honeycomb. Front Microbiol. 2017; 8: 1649, doi: 10.3389/fmicb.2017.01649.
  • Weston, RJ, Brocklebank, LK. The oligosaccharide composition of some New Zealand honeys. Food Chemistry. 1999; 64(1): 33-37, doi: 10.1016/s0308-8146(98)00099-5.
  • Xiong, ZR, Sogin, JH, Worobo, RW. Microbiome analysis of raw honey reveals important factors influencing the bacterial and fungal communities. Frontiers in Microbiology. 2022; 13: 1099522, doi: 10.3389/fmicb.2022.1099522.
  • Xu, P, Shi, M, Chen, XX. Antimicrobial peptide evolution in the Asiatic honey bee Apis cerana. Plos One. 2009; 4(3)(1): e4239, doi: 10.1371/journal.pone.0004239.
  • Zacharof, MP, Lovitt, RW. "Bacteriocins produced by lactic acid bacteria: A review article." In "APCBEE Procedia (ICBFS 2012: April 7-8, 2012, Bangkok, Thailand)". Vol. 2, 2012. p. 50-56. Print.
  • Zendo, T, Ohashi, C, Maeno, S, Piao, X, Salminen, S, Sonomoto, K, Endo, A, Zhang, YZ, Chen, YF, Wu, YQ, Si, JJ, Zhang, CP, Zheng, HQ, Hu, FL. Kunkecin A, a New Nisin Variant Bacteriocin Produced by the Fructophilic Lactic Acid Bacterium, Apilactobacillus kunkeei FF30-6 Isolated From Honey Bees Discrimination of the entomological origin of honey according to the secretions of the bee (Apis cerana or Apis mellifera). Frontiers in Microbiology. 2020; 11: 571903, doi: 10.3389/fmicb.2020.571903.
  • Zhang, YZ, Chen, YF, Wu, YQ, Si, JJ, Zhang, CP, Zheng, HQ, Hu, FL. Discrimination of the entomological origin of honey according to the secretions of the bee (Apis cerana or Apis mellifera). Food Research International. 2019; 116: 362-369, doi: 10.1016/j.foodres.2018.08.049.
  • Zhao, H, Cheng, N, Zhou, W, Chen, S, Wang, Q, Gao, H, Cao, W. Honey polyphenols ameliorate DSS-induced ulcerative colitis via modulating gut microbiota in rats. Molecular Nutrition & Food Research. 2019; 63(23): e1900638, doi: 10.1002/mnfr.201900638.
  • Zhao, X, Kuipers, OP. Identification and classification of known and putative antimicrobial compounds produced by a wide variety of Bacillales species. BMC Genomics. 2016; 17(1): 882, doi: 10.1186/s12864-016-3214-2.
  • Zheng, YZ, Deng, G, Liang, Q, Chen, DF, Guo, R, Lai, RC. Antioxidant activity of quercetin and its glucosides from propolis: A theoretical study. Scientific Reports. 2017; 7(1): 7543, doi: 10.1038/s41598-017-08024-8.

Balın Çok Yönlü Biyoaktivitesi: Arılar, Bitkiler Ve Mikroorganizmalar Arasındaki Etkileşimler

Year 2024, Volume: 24 Issue: 2, 356 - 385, 18.11.2024
https://doi.org/10.31467/uluaricilik.1511847

Abstract

Bal, antibakteriyel, anti-enflamatuar ve antioksidan aktiviteler gibi iyi belgelenmiş faydaları ile yüzyıllardır tıbbi özellikleriyle tanınmaktadır. Bununla birlikte, balın sağlıkla ilgili amaçlarla yaygın kullanımına rağmen, biyoaktivitesinden sorumlu olan altta yatan mekanizmaların çoğu yeterince araştırılmamıştır. Bu derleme, özellikle aktif maddelere ve bal mikrobiyomunun özelliklerine katkısına odaklanarak balın bileşiminin karmaşıklığını incelemektedir. Balın çok yönlü biyoaktivitesinin arılar, bitkiler ve mikroorganizmalar arasındaki etkileşimlerden nasıl kaynaklandığını anlamadaki boşluğu doldurmayı amaçlıyoruz. Bu derleme, balın sağlığa faydalarında hayati rol oynayan hidrojen peroksit, metilglioksal, polifenoller ve antimikrobiyal peptitler gibi temel bileşiklere ışık tutmaktadır. Ayrıca, nektarın bala kimyasal dönüşümünü birlikte etkileyen ve terapötik etkinliğini artıran bal arısının bağırsak mikrobiyomunun ve nektarın mikrobiyotasının genellikle göz ardı edilen katkılarını vurgulamaktadır. Bu makale, mevcut literatürü inceleyerek, çiçek kökeni, arı alt türleri ve çevresel koşullar gibi çeşitli faktörlerin balın tıbbi kalitesini nasıl etkilediğinin daha derinlemesine araştırılması gerektiğini vurgulamaktadır. Bu mekanizmaların anlaşılması, balın tıbbi uygulamalarda en uygun şekilde kullanılmasını sağlayabilir ve yeni terapötik potansiyelleri ortaya çıkarabilir. Bu makale, balı sadece besleyici bir gıda kaynağı değil aynı zamanda güçlü bir doğal ilaç yapan karmaşık süreçler ve bileşenler hakkında kapsamlı bir inceleme sunmaktadır.

Ethical Statement

Ethics committee approval is not required.

Supporting Institution

Russian Science Foundation (RSF)

Project Number

24-16-00179

Thanks

We thanks to Russian Science Foundation (RSF) grant 24-16-00179 for supporting our scientific research in Koltsov Institute of Developmental Biology at 2024.

References

  • Abdulgazina, NM, Farkhutdinov, RG, Yumaguzhin, FG, Veselov, DS. Comparative analysis of phytohormone content in nectar and honey collected by different breeds of bee. Modern Problems of Science and Education. 2015; (2-1): 17749, doi: 10.17513/spno.2015.2.
  • Abee, T, Klaenhammer, TR, Letellier, L. Kinetic studies of the action of lactacin F, a bacteriocin produced by Lactobacillus johnsonii that forms poration complexes in the cytoplasmic membrane. Applied and Environmental Microbiology. 1994; 60(3): 1006-1013, doi: 10.1128/aem.60.3.1006-1013.1994.
  • Abriouel, H, Franz, CMAP, Omar, NB, Gálvez, A. Diversity and applications of Bacillus bacteriocins. FEMS Microbiology Reviews. 2011; 35(1): 201-232, doi: 10.1111/j.1574-6976.2010.00244.x.
  • Alegría, Á, Delgado, S, Roces, C, López, B, Mayo, B. Bacteriocins produced by wild Lactococcus lactis strains isolated from traditional, starter-free cheeses made of raw milk. International Journal of Food Microbiology. 2010; 143(1-2): 61-66, doi: 10.1016/j.ijfoodmicro.2010.07.029.
  • Allison, GE, Worobo, RW, Stiles, ME, Klaenhammer, TR. Heterologous expression of the lactacin F peptides by Carnobacterium piscicola LV17. Applied and Environmental Microbiology. 1995; 61(4): 1371-1377, doi: 10.1128/aem.61.4.1371-1377.1995.
  • Al-Sheraji, SH, Ismail, A, Manap, MY, Mustafa, S, Yusof, RM, Hassan, FA. Prebiotics as functional foods: A review. Journal of Functional Foods. 2013; 5(4): 1542-1553, doi: 10.1016/j.jff.2013.08.009.
  • Alvarez-Pérez, S, Herrera, CM, de Vega, C. Zooming-in on floral nectar: A first exploration of nectar-associated bacteria in wild plant communities. FEMS Microbiology Ecology. 2012; 80(3): 591-602, doi: 10.1111/j.1574-6941.2012.01329.x.
  • Alvarez-Sieiro, P, Montalbán-López, M, Mu, D, Kuipers, OP. Bacteriocins of lactic acid bacteria: Extending the family. Applied Microbiology and Biotechnology. 2016; 100(7): 2939-2951, doi: 10.1007/s00253-016-7343-9.
  • Anderson, KE, Sheehan, TH, Mott, BM, Maes, P, Snyder, L, Schwan, MR, Corby-Harris, V. 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: e83125, doi: 10.1371/journal.pone.0083125.
  • Arredondo, D, Castelli, L, Porrini, MP, Garrido, PM, Eguaras, MJ, Zunino, P, Antunez, K. Lactobacillus kunkeei strains decreased the infection by honey bee pathogens Paenibacillus larvae and Nosema ceranae. Benef Microbes. 2018; 9(2): 279-290, doi: 10.3920/BM2017.0075.
  • Aumeeruddy, MZ, Zengin, G, Mahomoodally, MF. A review of the traditional and modern uses of Salvadora persica L. (Miswak): Toothbrush tree of Prophet Muhammad. Journal of Ethnopharmacology. 2018; 213: 409-444, doi: 10.1016/j.jep.2017.11.030.
  • Bachanova, K, Klaudiny, J, Kopernicky, J, Simuth, J. Identification of honeybee peptide active against Paenibacillus larvae larvae through bacterial growth-inhibition assay on polyacrylamide gel. Apidologie. 2002; 33(3): 259-269, doi: 10.1051/apido:2002015.
  • Balzan, MV, Sadula, R, Scalvenzi, L. Assessing ecosystem services supplied by agroecosystems in Mediterranean Europe: A literature review. Land. 2020; 9(8): 9-24, doi: 10.3390/land9080245.
  • Beretta, G, Caneva, E, Regazzoni, L, Bakhtyari, NG, Maffei Facino, R. A solid-phase extraction procedure coupled to 1H NMR, with chemometric analysis, to seek reliable markers of the botanical origin of honey. Analytica Chimica Acta. 2008; 620(1-2): 176-182, doi: 10.1016/j.aca.2008.05.025.
  • Berríos, P, Fuentes, JA, Salas, D, Carreño, A, Aldea, P, Fernández, F, Trombert, AN. Inhibitory effect of biofilm-forming Lactobacillus kunkeei strains against virulent Pseudomonas aeruginosa in vitro and in honeycomb moth (Galleria mellonella) infection model. Benef Microbes. 2018; 9(2): 257-268, doi: 10.3920/BM2017.0048.
  • Bleau, N, Bouslama, S, Giovenazzo, P, Derome, N. Dynamics of the honeybee (Apis mellifera) gut microbiota throughout the overwintering period in Canada. Microorganisms. 2020; 8(8): 1146, doi: 10.3390/microorganisms8081146.
  • 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): 677-689, doi: 10.1080/07315724.2008.10719745.
  • Bouzo, D, Cokcetin, NN, Li, L, Ballerin, G, Bottomley, AL, Lazenby, J, Whitchurch, CB, Paulsen, IT, Hassan, KA, Harry, EJ. Characterizing the mechanism of action of an ancient antimicrobial, manuka honey, against Pseudomonas aeruginosa using modern transcriptomics. mSystems. 2020; 5(3): e00106-e00120, doi: 10.1128%2FmSystems.00106-20.
  • Bovo, S, Ribani, A, Utzeri, VJ, Schiavo, G, Bertolini, F, Fontanesi, L. Shotgun metagenomics of honey DNA: Evaluation of a methodological approach to describe a multi-kingdom honey bee derived environmental DNA signature. Plos One. 2018; 13(10): e0205575, doi: 10.1371/journal.pone.0205575.
  • Bovo, S, Utzeri, VJ, Ribani, A, Cabbri, R, Fontanesi, L. Shotgun sequencing of honey DNA can describe honey bee derived environmental signatures and the honey bee hologenome complexity. Sci Rep. 2020; 10(1): 9279, doi: 10.1038/s41598-020-66127-1.
  • Brudzynski, K. A current perspective on hydrogen peroxide production in honey. A review. Food Chemistry. 2020; 332: 127229, doi: 10.1016/j.foodchem.2020.127229.
  • Brudzynski, K. Honey as an Ecological Reservoir of Antibacterial Compounds Produced by Antagonistic Microbial Interactions in Plant Nectars, Honey and Honey Bee. Antibiotics (Basel). 2021; 10(5): 551, doi: 10.3390/antibiotics10050551.
  • Brudzynski, K, Abubaker, K, Wang, T. Powerful bacterial killing by buckwheat honeys is concentration-dependent, involves complete DNA degradation and requires hydrogen peroxide. Front. Microbiol. 2012; 3: 242, doi: 10.3389/fmicb.2012.00242.
  • Brudzynski, K, Sjaarda, C. Antibacterial Compounds of Canadian Honeys Target Bacterial Cell Wall Inducing Phenotype Changes, Growth Inhibition and Cell Lysis That Resemble Action of β-Lactam Antibiotics. Plos One. 2014; 9(1): e106967, doi: 10.1371/journal.pone.0106967.
  • Brudzynski, K, Sjaarda, C. Honey Glycoproteins Containing Antimicrobial Peptides, Jelleins of the Major Royal Jelly Protein 1, Are Responsible for the Cell Wall Lytic and Bactericidal Activities of Honey. Plos One. 2015; 10(4): e0120238, doi: 10.1371/journal.pone.0120238.
  • Carter, C, Thornburg, RW. Is the nectar redox cycle a floral defense against microbial attack? Trends in Plant Science. 2004; 9(7): 320-324, doi: 10.1016/j.tplants.2004.05.008.
  • Carter, DA, Blair, SE, Cokcetin, NN, Bouzo, D, Brooks, P, Schothauer, R, Harry, EJ. Therapeutic manuka honey: No longer so alternative. Front Microbiol. 2016; 7: 569, doi: 10.3389/fmicb.2016.00569.
  • Casteels-Josson, K, Zhang, W, Capaci, T, Casteels, P, Tempst, P. Acute transcriptional response of the honey bees peptide-antibiotics gene repertoire, required posttranslational conversion of the precursor structures. Journal of Biological Chemistry. 1994; 269(44): 28569-28575, doi: 10.1016/S0021-9258(19)38548-0.
  • Caulier, S, Nannan, C, Gillis, A, Licciardi, F, Bragard, C, Mahillon, J. Overview of the Antimicrobial Compounds Produced by Members of the Bacillus subtilis Group. Frontiers in Microbiology. 2019; 10: 302, doi: 10.3389/fmicb.2019.00302.
  • Chanclud, E, Lacombe, B. Plant hormones: Key players in gut microbiota and human diseases? Trends in Plant Science. 2017; 22(9): 754-758, doi: 10.1016/j.tplants.2017.07.003.
  • Chauhan, SV, Chorawala, MR. Probiotics, prebiotics, and synbiotics. International Journal of Pharmaceutical Sciences and Research. 2014; 3(12): 711-726, doi: 10.1007/s13197-015-1921-1.
  • Chaven, S. "Chapter 11. Honey, Confectionery and Bakery Products." In "Food Safety Management". Ed. YL-l Motarjemi, H. Academic Press, Cambridge, MA, USA, 2014. p. 283-299. Print.
  • Chick, H, Shin, HS, Ustunol, Z. Growth and acid production by lactic acid bacteria and bifidobacteria grown in skim milk containing honey. Journal of Food Science. 2001; 66(3): 478-481, doi: 10.1111/j.1365-2621. 2001.tb16134.x.
  • Cho, H, Uehara, T, Bernhardt, TG. Beta-lactam antibiotics induce a lethal malfunctioning of the bacterial cell wall synthesis machinery. Cell. 2014; 159(6): 1300-1311, doi: 10.1016/j.cell.2014.11.017.
  • Chua, LS, Lee, JY, Chan, GF. Characterization of the proteins in honey. Analytical Letters. 2014; 48(4): 697-709, doi: 10.1080/00032719.2014.952374.
  • Combarros-Fuertes, P, Fresno, JM, Estevinho, MM, Sousa-Pimenta, M, Tornadijo, ME, Estevinho, LM. Honey: Another Alternative in the Fight against Antibiotic-Resistant Bacteria? Antibiotics (Basel). 2020; 9(11): 774, doi: 10.3390/antibiotics9110774.
  • Conway, PL, Stern, R, Tran, L. The Value-adding Potential of Prebiotic Components of Australian Honey). Rural Industries Research and Development Corporation, Barton, Australia, 2010, p. 30.
  • Corby-Harris, V, Maes, P, Anderson, KE. The bacterial communities associated with honey bee (Apis mellifera) foragers. Plos One. 2014; 9(4): e95056, doi: 10.1371/journal.pone.0095056.
  • da Silva, PM, Gauche, C, Gonzaga, LV, Costa, AC, Fett, R. Honey: Chemical composition, stability and authenticity. Food Chemistry. 2016; 196: 309-323, doi: 10.1016/j.foodchem.2015.09.051.
  • David, LA, Maurice, CF, Carmody, RN, Gootenberg, DB, Button, JE, Wolfe, BE, Ling, AV, Devlin, AS, Varma, Y, Fischbach, MA, Biddinger, SB, Dutton, RJ, Turnbaugh, PJ. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014; 505(7484): 559-563, doi: 10.1038/nature12820.
  • de Melo, FHC, Menezes, FNDD, de Sousa, JMB, dos Santos Lima, M, da Silva Campelo Borges, G, de Souza, EL, Magnani, M, International, FR. Prebiotic activity of monofloral honeys produced by stingless bees in the semi-arid region of Brazilian northeastern toward Lactobacillus acidophilus LA-05 and Bifidobacterium lactis BB-12. Food Research International. 2020; 128: 108809, doi: 10.1016/j.foodres.2019.108809.
  • De Vuyst, L, Leroy, F. Bacteriocins from lactic acid bacteria: Production, purification, and food applications. Journal of Molecular Microbiology and Biotechnology. 2007; 13(4): 194-199, doi: 10.1159/000104752.
  • Deleu, M, Lorent, J, Lins, L, Brasseur, R, Braun, N, El Kirat, K, Nylander, T, Dufrêne, YF, Mingeot-Leclercq, MP. Effects of surfactin on membrane models displaying lipid phase separation. Biochimica et Biophysica Acta. 2013; 1828(2): 801-815, doi: 10.1016/j.bbamem.2012.11.007.
  • Deshmukh, SK, Verekar, SA, Bhave, SV. Endophytic fungi: A reservoir of antibacterials. Frontiers in Microbiology. 2015; 5: 715, doi: 10.3389/fmicb.2014.00715.
  • Di Girolamo, F, D'Amato, A, Righetti, PG. Assessment of the floral origin of honey via proteomic instruments. Journal of Proteomics. 2012; 75(12): 3688-3693, doi: 10.1016/j.jprot.2012.04.029.
  • Disayathanoowat, T, Li, H, Supapimon, N, Suwannarach, N, Lumyong, S, Chantawannakul, P, Guo, J. Different dynamics of bacterial and fungal communities in hive-stored bee bread and their possible roles: A case study from two commercial honey bees in China. Microorganisms. 2020; 8(2): 264, doi: 10.3390/microorganisms8020264.
  • Dong, ZX, Li, HY, Chen, YF, Wang, F, Deng, XY, Lin, LB, Zhang, QL, Li, J, Guo, J. Colonization of the gut microbiota of honey bee (Apis mellifera) workers at different developmental stages. Microbiol Res. 2020; 231: 126370, doi: 10.1016/j.micres.2019.126370.
  • Elzeini, HM, Ali, A, Nasr, NF, Hassan, M, Hassan, AAM, Elenany, YE. Probiotic capability of novel lactic acid bacteria isolated from worker honey bees gut microbiota. FEMS Microbiology Letters. 2021; 368(6): fnab030, doi: 10.1093/femsle/fnab030.
  • Endo, A, Salminen, S. Honeybees and beehives are rich sources for fructophilic lactic acid bacteria. Systematic and Applied Microbiology. 2013; 36(6): 444-448, doi: 10.1016/j.syapm.2013.05.011.
  • Erban, T, Shcherbachenko, E, Talacko, P, Harant, K. The Unique Protein Composition of Honey Revealed by Comprehensive Proteomic Analysis: Allergens, Venom-like Proteins, Antibacterial Properties, Royal Jelly Proteins, Serine Proteases, and Their Inhibitors. Journal of Natural Products. 2019; 82(5): 1217-1226, doi: 10.1021/acs.jnatprod.8b01061.
  • Evans, JD, Aronstein, K, Chen, YP, Hetru, C, Imler, JL, Jiang, H, Kanost, M, Thompson, GJ, Zou, Z, Hultmark, D. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Molecular Biology. 2006; 15(5): 645-656, doi: 10.1111/j.1365-2583.2006.00682.x.
  • Forsgren, E, Olofsson, TC, Vásquez, A, Fries, I. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie. 2009; 41(1): 99-108, doi: 10.1051/apido/2009065.
  • Fuandila, NN, Widanarni, W, Yuhana, M. Growth performance and immune response of prebiotic honey fed Pacific white shrimp Litopenaeus vannamei to Vibrio parahaemolyticus infection. Journal of Applied Aquaculture. 2019; 32(3): 221-235, doi: 10.1080/10454438.2019.1615593.
  • Fujiwara, S, Imai, J, Fujiwara, M, Yaeshima, T, Kawashima, T, Kobayashi, K. A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. Journal of Biological Chemistry. 1990; 265(19): 11333-11337, doi: 10.1016/S0021-9258(19)38596-5.
  • Genersch, E. American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. Journal of Invertebrate Pathology. 2010; 103: S10-S19, doi: 10.1016/j.jip.2009.06.015.
  • Gibson, GR, Roberfroid, MB. Dietary modulation of the human colonic microbiota: Introducing the concept of prebiotics. Journal of Nutrition. 1995; 125(6): 1401-1412, doi: 10.1093/jn/125.6.1401.
  • Gong, HS, Meng, XC, Wang, H. Mode of action of plantaricin MG, a bacteriocin active against Salmonella typhimurium. Journal of Basic Microbiology. 2010; 50(1): S37-S45, doi: 10.1002/jobm.200900307.
  • Gou, W, Fu, Y, Yue, L, Chen, G-d, Cai, X, Shuai, M, Xu, F, Yi, X, Chen, H, Zhu, Y, Xiao, M-l, Jiang, Z, Miao, Z, Xiao, C, Shen, B, Wu, X, Zhao, H, Ling, W, Wang, J, Chen, Y-m, Guo, T, Zheng, J-S. Gut microbiota may underlie the predisposition of healthy individuals to COVID-19. Research square. 2020; 1: 1-24, doi: 10.21203/rs.3.rs-45991/v1.
  • Grady, EN, MacDonald, J, Liu, L, Richman, A, Yuan, ZC. Current knowledge and perspectives of Paenibacillus: A review. Microb Cell Fact. 2016; 15(1): 203, doi: 10.1186/s12934-016-0603-7.
  • Haddadin, MSY, Jamal Abu, INS, Robinson, RK. Effect of honey on the growth and metabolism of two bacterial species of intestinal origin. Pakistan Journal of Nutrition. 2007; 6(6): 693-697, doi: 10.3923/pjn.2007.693.697.
  • Hamayun, M, Hussain, A, Khan, SA, Kim, HY, Khan, AL, Waqas, M, Irshad, M, Iqbal, A, Rehman, G, Jan, S, Lee, IJ. Gibberellins producing endophytic fungus Porostereum spadiceum AGH786 rescues growth of salt-affected soybean. Front Microbiol. 2017; 8: 686, doi: 10.3389/fmicb.2017.00686.
  • Hammond, EN, Donkor, ES. Antibacterial effect of manuka honey on Clostridium difficile. BMC Research Notes. 2013; 6: 188, doi: 10.1186/1756-0500-6-188.
  • Hasyimi, W, Widanarni, W, Yuhana, M. Growth performance and intestinal microbiota diversity in Pacific white shrimp Litopenaeus vannamei fed with a probiotic bacterium, honey prebiotic, and synbiotic. Current Microbiology. 2020; 77(10): 2982-2990, doi: 10.1007/s00284-020-02117-w.
  • Henriques, AF, Jenkins, RE, Burton, NF, Cooper, RA. The effect of manuka honey on the structure of Pseudomonas aeruginosa. European Journal of Clinical Microbiology & Infectious Diseases. 2011; 30(2): 167-171, doi: 10.1007/s10096-010-1073-y.
  • Herold, E, Leibold, G. Heilwerte aus dem Bienenvolk). Kosmos (Franckh-Kosmos), Germany, 2000, p.
  • Hiel, S, Bindels, LB, Pachikian, BD, Kalala, G, Broers, V, Zamariola, G, Chang, BPI, Kambashi, B, Rodriguez, J, Cani, PD, Neyrinck, AM, Thissen, JP, Luminet, O, Bindelle, J, Delzenne, NM. Effects of a diet based on inulin-rich vegetables on gut health and nutritional behavior in healthy humans. American Journal of Clinical Nutrition. 2019; 109(6): 1683-1695, doi: 10.1093/ajcn/nqz001.
  • Hilgarth, M, Redwitz, J, Ehrmann, MA, Vogel, RF, Jakob, F. Bombella favorum sp. Nov. And Bombella mellum sp. Nov., two novel species isolated from the honeycombs of Apis mellifera. Int J Syst Evol Microbiol. 2021; 71(2): 10.1099/ijsem.1090.004633, doi: 10.1099/ijsem.0.004633.
  • Ilyasov, RA, Nikolenko, AG, Saifullina, N. Dark forest bee Apis mellifera mellifera L. of the Republic of Bashkortostan). Gilem, Bashkortostan Encyclical, Ufa, Russia, 2015, p. 308.
  • Isah, T. Stress and defense responses in plant secondary metabolites production. Biol. Res. 2019; 52(1): 39, doi: 10.1186/s40659-019-0264-y.
  • Jack, RW, Tagg, JR, Ray, B. Bacteriocins of Gram-positive bacteria. Microbiological Reviews. 1995; 59(2): 171, doi: 10.1128/mr.59.2.171-200.1995.
  • Janek, T, Drzymała, K, Dobrowolski, A. In vitro efficacy of the lipopeptide biosurfactant surfactin-C15 and its complexes with divalent counterions to inhibit Candida albicans biofilm and hyphal formation. Bio-fouling. 2020; 36: 210-221, doi: 10.1080/08927014.2020.1720453.
  • Jiang, L, Xie, M, Chen, G, Qiao, J, Zhang, H, Zeng, X. Phenolics and carbohydrates in buckwheat honey regulate the human intestinal microbiota. JF. Ecology and Evolution. 2020; 8: 6432942, doi: 10.1155/2020/6432942.
  • Johnston, M, McBride, M, Dahiya, D, Owusu-Apenten, R, Nigam, PS. Antibacterial activity of Manuka honey and its components: An overview. AIMS microbiology. 2018; 4(4): 655-664, doi: 10.3934/microbiol.2018.4.655.
  • Jones, JC, Fruciano, C, Hildebrand, F, Al Toufalilia, H, Balfour, NJ, Bork, P, Engel, P, Ratnieks, FLW, Hughes, WOH. Gut microbiota composition is associated with environmental landscape in honey bees. Ecology and Evolution. 2017; 8(1): 441-451, doi: 10.1002/ece3.3597.
  • Kačániová, M, Pavlicova, S, Hascik, P, Kociubinski, G, Knazovicka, V, Sudzina, M, Sudzinova, J, Fikselova, M. Microbial communities in bees, pollen and honey from Slovakia. Acta Microbiologica et Immunologica Hungarica. 2009; 56(3): 285-295, doi: 10.1556/AMicr.56.2009.3.7.
  • Kafantaris, I, Amoutzias, GD, Mossialos, D. Foodomics in bee product research: A systematic literature review. European Food Research and Technology. 2020; 247(2): 309-331, doi: 10.1007/s00217-020-03634-5.
  • Karabagias, IK. A targeted metabolomic procedure for the identification of isophorone-related compounds in honey. Journal of Plant Biochemistry & Physiology. 2018; 6(01): 10.4172/2329-9029.1000210, doi: 10.4172/2329-9029.1000210.
  • Keller, A, Brandel, A, Becker, MC, Balles, R, Abdelmohsen, UR, Ankenbrand, MJ, Sickel, W. Wild bees and their nests host Paenibacillus bacteria with functional potential of avail. Microbiome. 2018; 6(1): 229, doi: 10.1186/s40168-018-0614-1.
  • Kešnerová, L, Emery, O, Troilo, M, Liberti, J, Erkosar, B, Engel, P. Gut microbiota structure differs between honeybees in winter and summer. ISME J. 2020; 14(3): 801-814, doi: 10.1038/s41396-019-0568-8.
  • 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): 414-421, doi: 10.1099/ijsem.0.000736.
  • Khalil, MI, Alam, N, Moniruzzaman, M, Sulaiman, SA, Gan, SH. Phenolic acid composition and antioxidant properties of Malaysian honeys. Journal of Food Science. 2011; 76(6): C921-928, doi: 10.1111/j.1750-3841.2011.02282.x.
  • Khan, A, Doshi, HV, Thakur, MC. "Bacillus spp.: A Prolific Siderophore Producer." In "Bacilli and Agrobiotechnology". Ed. MR Islam, M. Pandey, P. Jha, C. Aeron, A. Springer, Cham, Switzerland, 2016. p. 255. Print.
  • Klaudiny, J, Albert, S, Bachanová, K, Kopernický, J, Šimúth, J. Two structurally different defensin genes, one of them encoding a novel defensin isoform, are expressed in honeybee Apis mellifera. Insect Biochemistry and Molecular Biology. 2005; 35(1): 11-22, doi: 10.1016/j.ibmb.2004.09.007.
  • Kňazovická, V. Diversity of Bacteria in Slovak and Foreign Honey, with Assessment of Its Physico-Chemical Quality and Counts of Cultivable Microorganisms. Journal of Microbiology, Biotechnology and Food Sciences. 2019; 9(Special issue): 414-421, doi: 10.15414/jmbfs.2019.9.special.414-421.
  • Kolayli, S, Boukraâ, L, Sahin, H, Abdellah, F. "Sugars in honey." In "Dietary sugars: chemistry, analysis, function and effects". Ed. VR Preedy. The Royal Society of Chemistry, Cambridge, UK, 2012. p. 3-15. Print.
  • Kurek-Gorecka, A, Gorecki, M, Rzepecka-Stojko, A, Balwierz, R, Stojko, J. Bee products in dermatology and skin care. Molecules. 2020; 25(3): 10.3390/molecules25030556, doi: 10.3390/molecules25030556.
  • Kwakman, PH, te Velde, AA, de Boer, L, Speijer, D, Vandenbroucke-Grauls, CM, Zaat, SA. How honey kills bacteria. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2010; 24(7): 2576-2582, doi: 10.1096/fj.09-150789.
  • Lebedev, VI, Murashova, EA. Influence of breed and placement of brood on the quality of honey. Russian Journal of Beekeeping " Pchelovodstvo". 2004; (3): 50-52, doi:
  • Lee, H, Churey, JJ, Worobo, RW. Purification and structural characterization of bacillomycin F produced by a bacterial honey isolate active against Byssochlamys fulva H25. Journal of Applied Microbiology. 2008; 105(3): 663-673, doi: 10.1111/j.1365-2672.2008.03797.x.
  • Lee, H, Churey, JJ, Worobo, RW. Biosynthesis and transcriptional analysis of thurincin H, a tandem repeated bacteriocin genetic locus, produced by Bacillus thuringiensis SF361. FEMS Microbiology Letters. 2009; 299(2): 205-213, doi: 10.1111/j.1574-6968.2009.01749.x.
  • Lee, JH, Park, JH, Kim, JA, Neupane, GP, Cho, MH, Lee, CS, Lee, J. Low concentrations of honey reduce biofilm formation, quorum sensing, and virulence in Escherichia coli O157:H7. Biofouling. 2011; 27(10): 1095-1104, doi: 10.1080/08927014.2011.633704.
  • Leeming, ER, Johnson, AJ, Spector, TD, Le Roy, CI. Effect of Diet on the Gut Microbiota: Rethinking Intervention Duration. Nutrients. 2019; 11(12): 2862, doi: 10.3390/nu11122862.
  • Li, Y, Long, S, Liu, Q, Ma, H, Li, J, Xiaoqing, W, Yuan, J, Li, M, Hou, B. Gut microbiota is involved in the alleviation of loperamide-induced constipation by honey supplementation in mice. Food Sci Nutr. 2020; 8(8): 4388-4398, doi: 10.1002/fsn3.1736.
  • Liu, GL, Chi, Z, Wang, GY, Wang, ZP, Li, Y, Chi, ZM. Yeast killer toxins, molecular mechanisms of their action and their applications. Critical Reviews in Biotechnology. 2015; 35: 222–234, doi: 10.3109/07388551.2013.879318.
  • Luong, DV, Tam, NQ, Xuan, DTT, Tai, NT. NMR based metabolomic approach for evaluation of Vietnamese honey. Vietnam Journal of Chemistry. 2019; 57(6): 712-716, doi: 10.1002/vjch.2019000101.
  • Machado De-Melo, A, De Almeida-Muradian, L, Sancho, M, Pascual Maté, A. Composition and properties of Apis mellifera honey: A review. Journal of Apicultural Research. 2017; 57(1): 1-33, doi: 10.1080/00218839.2017.1338444.
  • Maddocks, SE, Jenkins, RE. Honey: A sweet solution to the growing problem of antimicrobial resistance? Future Microbiology. 2013; 8(11): 1419-1429, doi: 10.2217/fmb.13.105.
  • Martinson, VG, Moy, J, Moran, NA. Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol. 2012; 78(8): 2830-2840, doi: 10.1128/AEM.07810-11.
  • 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. Mol. Nutr. Food Res. 2008; 52(4): 483-489, doi: 10.1002/mnfr.200700282.
  • McAuliffe, OR, Ross, P, Hill, C. Lantibiotics: Structure, biosynthesis and mode of action. FEMS Microbiology Reviews. 2001; 25(3): 285-308, doi: 10.1111/j.1574-6976.2001.tb00579.x.
  • Meng, F, Liu, Y, Nie, T, Tang, C, Lyu, F, Bie, X, Lu, Y, Zhao, M, Lu, Z. Plantaricin A, Derived from Lactiplantibacillus plantarum, Reduces the Intrinsic Resistance of Gram-Negative Bacteria to Hydrophobic Antibiotics. Applied and Environmental Microbiology. 2022; 88(10): e0037122, doi: 10.1128/aem.00371-22.
  • Miethke, M, Klotz, O, Linne, U, May, JJ, Beckering, CL, Marahiel, MA. Ferri-bacillibactin uptake and hydrolysis in Bacillus subtilis. Molecular Microbiology. 2006; 61(6): 1413-1427, doi: 10.1111/j.1365-2958.2006.05321.x.
  • Miguel, MG, Antunes, MD, Faleiro, ML. Honey as a complementary medicine. Integrative Medicine Insights. 2017; 12: 1178633717702869, doi: 10.1177/1178633717702869.
  • Mohan, A, Quek, S-Y, Gutierrez-Maddox, N, Gao, Y, Shu, Q. Effect of honey in improving the gut microbial balance. Food Quality and Safety. 2017; 1(2): 107-115, doi: 10.1093/fqsafe/fyx015.
  • Muhialdin, BJ, Hassan, Z, Saari, N. In vitro antifungal activity of lactic acid bacteria low molecular peptides against spoilage fungi of bakery products. Annals of Microbiology. 2018; 68(8): 557-567, doi: 10.1007/s13213-018-1332-8.
  • Mukherjee, A, Gaurav, AK, Singh, S, Yadav, S, Bhowmick, S, Abeysinghe, S, Verma, JP. The bio-active potential of phytohormones: A review. Biotechnology Reports. 2022; 35: e00748, doi: 10.1016/j.btre.2022.e00748.
  • Nagpal, R, Kaur, A. Synbiotic effect of various prebiotics on in vitro activities of probiotic Lactobacilli. Ecology of Food and Nutrition. 2011; 50(1): 63-68, doi: 10.1080/03670244.2011.539161.
  • Naseer, S, Khan, S, Azim, K. Identification of cultivable bacteria from natural honey of different botanical origin. Pakistan Journal of Biochemistry and Molecular Biology. 2015; 48: 53-56, doi:
  • Nolan, VC, Harrison, J, Cox, JAG. Dissecting the Antimicrobial Composition of Honey. Antibiotics (Basel). 2019; 8(1): 251, doi: 10.3390/antibiotics8040251.
  • Nooh, HZ, Nour-Eldien, NM. The anti dual-inflammatory and antioxidant activities of natural honey promote cell proliferation and neural regeneration in a rat model of colitis. Acta Histochem. 2016; 118(6): 588-595, doi: 10.1016/j.acthis.2016.06.006.
  • Nowak, A, Szczuka, D, Gorczynska, A, Motyl, I, Kregiel, D. Characterization of Apis mellifera gastrointestinal microbiota and lactic acid bacteria for honeybee protection—a review. Cells. 2021; 10(3): 701, doi: 10.3390/cells10030701.
  • Olaitan, PB, Adeleke, OE, Ola, IO. Honey: A reservoir for microorganisms and an inhibitory agent for microbes. African Health Sciences. 2007; 7(3): 159-165, doi: 10.5555/afhs.2007.7.3.159.
  • Olawode, EO, Tandlich, R, Cambray, G. (1)H-NMR Profiling and Chemometric Analysis of Selected Honeys from South Africa, Zambia, and Slovakia. Molecules. 2018; 23(3)doi: 10.3390/molecules23030578.
  • Olofsson, TC, Alsterfjord, M, Nilson, B, Butler, E, Vázquez, 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(Pt 9): 3109-3119, doi: 10.1099/ijs.0.059600-0.
  • Olofsson, TC, Butler, E, Markowicz, P, Lindholm, C, Larsson, L, Vázquez, A. Lactic bacterial acid symbionts in honeybees - an unknown key to honey's antimicrobial and therapeutic activities. International Wound Journal. 2016; 13(5): 668-679, doi: 10.1111/iwj.12345.
  • Olofsson, TC, Vasquez, 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): 356-363, doi: 10.1007/s00284-008-9202-0.
  • Oscáriz, JC, Pisabarro, AG. Classification and mode of action of membrane-active bacteriocins produced by gram-positive bacteria. International Microbiology. 2001; 4(1): 13-19, doi: 10.1007/s10123-001-0056-y.
  • Pajor, M, Worobo, RW, Milewski, S, Szweda, P. The Antimicrobial Potential of Bacteria Isolated from Honey Samples Produced in the Apiaries Located in Pomeranian Voivodeship in Northern Poland. International Journal of Environmental Research and Public Health. 2018; 15(9)doi: 10.3390/ijerph15092002.
  • Pajor, M, Xiong, ZR, Worobo, RW, Szweda, P. Paenibacillus alvei MP1 as a Producer of the Proteinaceous Compound with Activity against Important Human Pathogens, Including Staphylococcus aureus and Listeria monocytogenes. Pathogens. 2020; 9(4): 319, doi: 10.3390/pathogens9040319.
  • Parada, JL, Caron, CR, Medeiros, ABP, Soccol, CR. Bacteriocins from lactic acid bacteria: Purification, properties and use as biopreservatives. Brazilian Archives of Biology and Technology. 2007; 50(4): 521–542, doi: 10.1590/S1516-89132007000300018
  • Paraszkiewicz, K, Moryl, M, Płaza, G, Bhagat, D, Satpute, SK, Bernat, P. Surfactants of microbial origin as antibiofilm agents. International Journal of Environmental Health Research. 2019; 31: 401-420, doi: 10.1080/09603123.2019.1579732.
  • Poirel, L, Jayol, A, Nordmann, P. Polymyxins: Antibacterial Activity, Susceptibility Testing, and Resistance Mechanisms Encoded by Plasmids or Chromosomes. Clinical Microbiology Reviews. 2017; 30(2): 557-596, doi: 10.1128/CMR.00064-16.
  • Pomastowski, P, Zloch, M, Rodzik, A, Ligor, M, Kostrzewa, M, Buszewski, B. Analysis of bacteria associated with honeys of different geographical and botanical origin using two different identification approaches: MALDI-TOF MS and 16S rDNA PCR technique. Plos One. 2019; 14(5): e0217078, doi: 10.1371/journal.pone.0217078.
  • Popa, D, Ustunol, Z. Influence of sucrose, high fructose corn syrup and honey from different floral sources on growth and acid production by lactic acid bacteria and bifidobacteria. International Journal of Dairy Technology. 2011; 64(2): 247-253, doi: 10.1111/j.1471-0307.2011.00666.x.
  • 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(4): 1248-1260, doi: 10.1111/jam.14469.
  • Ranneh, Y, Akim, AM, Hamid, HA, Khazaai, H, Fadel, A, Zakaria, ZA, Albujja, M, Bakar, MFA. Honey and its nutritional and anti-inflammatory value. BMC Complement Med Ther. 2021; 21(1): 30, doi: 10.1186/s12906-020-03170-5.
  • Raschka, L, Daniel, H. Mechanisms underlying the effects of inulin-type fructans on calcium absorption in the large intestine of rats. Bone. 2005; 37(5): 728-735, doi: 10.1016/j.bone.2005.05.015.
  • Raymann, K, Bobay, LM, Moran, NA. Antibiotics reduce genetic diversity of core species in the honeybee gut microbiome. Molecular Ecology. 2018; 27(8): 2057-2066, doi: 10.1111/mec.14434.
  • Raymann, K, Shaffer, Z, Moran, NA. Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biology. 2017; 15(3): e2001861, doi: 10.1371/journal.pbio.2001861.
  • Rea, MC, Sit, CS, Clayton, E, O’Connor, PM, Whittal, RM, Zheng, J, Vederas, JC, Ross, RP, Hill, C, Rutherford, ST, Bassler, BL. Thuricin CD, a posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile Bacterial quorum sensing: Its role in virulence and possibilities for its control. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(20): 9352-9357, doi: 10.1073/pnas.0913554107.
  • Roberfroid, M, Gibson, GR, Hoyles, L, McCartney, AL, Rastall, R, Rowland, I, Wolvers, D, Watzl, B, Szajewska, H, Stahl, B, Guarner, F, Respondek, F, Whelan, K, Coxam, V, Davicco, MJ, Leotoing, L, Wittrant, Y, Delzenne, NM, Cani, PD, Neyrinck, AM, Meheust, A. Prebiotic effects: Metabolic and health benefits. British Journal of Nutrition. 2010; 104 Suppl 2: S1-S63, doi: 10.1017/S0007114510003363.
  • Rodríguez-Andrade, E, Stchigel, AM, Terrab, AJ, Guarro, A, Cano-Lira, JF. Diversity of xerotolerant and xerophilic fungi in honey. IMA Fungus. 2019; 10(1): 20, doi: 10.1186/s43008-019-0017-6.
  • Rosendale, DI, Maddox, IS, Miles, MC, Rodier, M, Skinner, M, Sutherland, J. High-throughput microbial bioassays to screen potential New Zealand functional food ingredients intended to manage the growth of probiotic and pathogenic gut bacteria. International Journal of Food Science & Technology. 2008; 43(12): 2257-2267, doi: 10.1111/j.1365-2621.2008.01863.x.
  • Rutherford, ST, Bassler, BL. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harbor Perspectives in Medicine. 2012; 2(11)doi: 10.1101/cshperspect.a012427.
  • Sadiq, FA, Yan, B, Tian, F, Zhao, J, Zhang, H, Chen, W. Lactic Acid Bacteria as Antifungal and Anti-Mycotoxigenic Agents: A Comprehensive Review. Comprehensive Reviews in Food Science and Food Safety. 2019; 18(5): 1403-1436, doi: 10.1111/1541-4337.12471.
  • Samaranayaka, AGP, Li-Chan, ECY. Food-derived peptidic antioxidants: A review of their production, assessment, and potential applications. Journal of Functional Foods. 2011; 3(4): 229-254, doi: 10.1016/j.jff.2011.05.006.
  • Sanz, ML, González, M, de Lorenzo, C, Sanz, J, Martínez-Castro, I. Carbohydrate composition and physicochemical properties of artisanal honeys from Madrid (Spain): Occurrence of Echium sp honey. Journal of the Science of Food and Agriculture. 2004; 84(12): 1577-1584, doi: 10.1002/jsfa.1823.
  • Sanz, ML, Polemis, N, Morales, V, Corzo, N, Drakoularakou, A, Gibson, GR, Rastall, RA. In vitro investigation into the potential prebiotic activity of honey oligosaccharides. Journal of Agricultural and Food Chemistry. 2005; 53(8): 2914-2921, doi: 10.1021/jf0500684.
  • Scarfi, S, Ferraris, C, Fruscione, F, Fresia, C, Guida, L, Bruzzone, S, Usai, C, Parodi, A, Millo, E, Salis, A, Burastero, G, De Flora, A, Zocchi, E. Cyclic ADP ribose-mediated expansion and stimulation of human mesenchymal stem cells by the plant hormone abscisic acid. Stem Cells. 2008; 26(11): 2855-2864, doi: 10.1634/stemcells.2008-0488.
  • Schell, KR, Fernandes, KE, Shanahan, E, Wilson, I, Blair, SE, Carter, DA, Cokcetin, NN. The potential of honey as a prebiotic food to re-engineer the gut microbiome toward a healthy state. Frontiers in Nutrition. 2022; 9: 957932, doi: 10.3389/fnut.2022.957932.
  • Schramm, DD, Karim, M, Schrader, HR, Holt, RR, Cardetti, M, Keen, CL. Honey with high levels of antioxidants can provide protection to healthy human subjects. Journal of Agricultural and Food Chemistry. 2003; 51(6): 1732-1735, doi: 10.1021/jf025928k.
  • Seraglio, SKT, Silva, B, Bergamo, G, Brugnerotto, P, Gonzaga, LV, Fett, R, Costa, ACO. An overview of physicochemical characteristics and health-promoting properties of honeydew honey. Food Research International. 2019; 119: 44-66, doi: 10.1016/j.foodres.2019.01.028.
  • Sharma, D, Saharan, BS. Functional characterization of biomedical potential of biosurfactant produced by Lactobacillus helveticus. Biotechnology Reports. 2016; 11: 27-35, doi: 10.1016/j.btre.2016.08.005.
  • Shin, HS, Ustunol, Z. Carbohydrate composition of honey from different floral sources and their influence on the growth of selected intestinal bacteria: An in vitro comparison. Food Research International. 2005; 38(6): 721-728, doi: 10.1016/j.foodres.2005.01.007.
  • Sinacori, M, Francesca, N, Alfonzo, A, Cruciata, M, Sannino, C, Settanni, L, Moschetti, G. Cultivable microorganisms associated with honeys of different geographical and botanical origin. Food Microbiology. 2014; 38: 284-294, doi: 10.1016/j.fm.2013.07.013.
  • Slačanac, V, Lučan, M, Hardi, J, Krstanović, V, Koceva Komlenić, D. Fermentation of honey-sweetened soymilk with Bifidobacterium lactis Bb-12 and Bifidobacterium longum Bb-46: fermentation activity of bifidobacteria and in vitro antagonistic effect against Listeria monocytogenes FSL N1-017. Czech Journal of Food Sciences. 2012; 30(4): 321-329, doi: 10.17221/190/2011-CJFS.
  • Snowdon, JA, Cliver, DO. Microorganisms in honey. International Journal of Food Microbiology. 1996; 31(1-3): 1-26, doi: 10.1016/0168-1605(96)00970-1.
  • Sood, S, Steinmetz, H, Beims, H, Mohr, KI, Stadler, M, Djukic, M, von der Ohe, W, Steinert, M, Daniel, R, Müller, R. Paenilarvins: Iturin family lipopeptides from the honey bee pathogen Paenibacillus larvae. ChemBioChem. 2014; 15(13): 1947-1955, doi: 10.1002/cbic.201402139.
  • Straight, PD, Fischbach, MA, Walsh, CT, Rudner, DZ, Kolter, R. A singular enzymatic mega-complex from Bacillus subtilis. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104: 305-310, doi: 10.1073/pnas.0609073104.
  • Sudisha, J, Sharathchandra, RG, Amruthesh, KN, Kumar, A, Shetty, HS. "Pathogenesis Related Proteins in Plant Defense Response." In "Plant Defence: Biological Control. Progress in Biological Control". 2011. p. 12. Print.
  • Sumi, CD, Yang, BW, Yeo, IC, Hahm, YT. Antimicrobial peptides of the genus Bacillus: A new era for antibiotics. Canadian Journal of Microbiology. 2015; 61(2): 93-103, doi: 10.1139/cjm-2014-0613.
  • Tanes, C, Bittinger, K, Gao, Y, Friedman, ES, Nessel, L, Paladhi, UR, Chau, L, Panfen, E, Fischbach, MA, Braun, J, Xavier, RJ, Clish, CB, Li, H, Bushman, FD, Lewis, JD, Wu, GD. Role of dietary fiber in the recovery of the human gut microbiome and its metabolome. Cell Host Microbe. 2021; 29(3): 394-407, doi: 10.1016/j.chom.2020.12.012.
  • Tiihonen, K, Ouwehand, AC, Rautonen, N. Human intestinal microbiota and healthy ageing. Ageing Res Rev. 2010; 9(2): 107-116, doi: 10.1016/j.arr.2009.10.004.
  • Tola, YH, Waweru, JW, Hurst, GDD, Slippers, B, Paredes, JC. Characterization of the Kenyan honey bee (Apis mellifera) gut microbiota: A first look at tropical and sub-Saharan African bee-associated microbiomes. Microorganisms. 2020; 8(11): 1721, doi: 10.3390/microorganisms8111721.
  • Turski, MP, Turska, M, Zgrajka, W, Kuc, D, Turski, WA. Presence of kynurenic acid in food and honeybee products. Amino Acids. 2009; 36(1): 75-78, doi: 10.1007/s00726-008-0031-z.
  • Upreti, GC, Hinsdill, RD. Production and mode of action of lactocin 27: Bacteriocin from a homofermentative Lactobacillus. Antimicrobial Agents and Chemotherapy. 1975; 7(2): 139-145, doi: 10.1128/aac.7.2.139.
  • Vakhonina, TV. Bee pharmacy). Institute of Beekeeping, Rybnoye, Russia, 2002, p. 190.
  • Vallianou, NG. Honey and its anti-inflammatory, anti-bacterial, and anti-oxidant properties. General Medicine. 2014; 02(02): 132, doi: 10.4172/2327-5146.1000132.
  • Vásquez, A, Forsgren, E, Fries, I, Paxton, RJ, Flaberg, E, Szekely, L, Olofsson, TC. Symbionts as major modulators of insect health: Lactic acid bacteria and honeybees. Plos One. 2012; 7(3): e33188, doi: 10.1371/journal.pone.0033188.
  • Vásquez, A, Olofsson, TC. The lactic acid bacteria involved in the production of bee pollen and bee bread. Journal of Apicultural Research. 2009; 48(3): 189-195, doi: 10.3896/Ibra.1.48.3.07.
  • Venkatesh, N, Keller, NP. Mycotoxins in Conversation with Bacteria and Fungi. Frontiers in Microbiology. 2019; 10: 403, doi: 10.3389/fmicb.2019.00403.
  • Vlamakis, H, Chai, Y, Beauregard, P, Losick, R, Kolter, R. Sticking together: Building a biofilm the Bacillus subtilis way. Nature Reviews Microbiology. 2013; 11(3): 157-168, doi: 10.1038/nrmicro2960.
  • Voller, J, Maková, B, Kadlecová, A, Gonzalez, G, Strnad, M. "Plant hormone cytokinins for modulating human aging and age-related diseases." In "Hormones in Ageing and Longevity". Ed. SS Rattan, Ramesh. Springer Cham, Cham, Germany, 2017. p. 311-335. Print.
  • Vrabie, V, Yazlovitska, L, Ciochină, V, Rotaru, S. Comparative content of free amino acids in pollen and honey. Bulletin Ştiinţific. Revista de Etnografie, Ştiinţele Naturii şi Muzeologie (Serie Nouă). 2019; 30(43): 71-78, doi:
  • Wang, K, Li, J, Zhao, L, Mu, X, Wang, C, Wang, M, Wu, L. Gut microbiota protects honey bees (Apis mellifera L.) against polystyrene microplastics exposure risks. Journal of Hazardous Materials. 2021; 402: 123828, doi: 10.1016/j.jhazmat.2020.123828.
  • Wang, K, Wan, ZR, Ou, AQ, Liang, XW, Guo, XX, Zhang, ZY, Xue, XF. Monofloral honey from a medical plant, Prunella vulgaris, protected against dextran sulfate sodium-induced ulcerative colitis via modulating gut microbial populations in rats. Food & Function. 2019; 10(7): 3828-3838, doi: 10.1039/c9fo00460b.
  • Wang, Q, Cai, WJ, Yu, L, Ding, J, Feng, YQ. Comprehensive profiling of phytohormones in honey by sequential liquid-liquid extraction coupled with liquid chromatography-mass spectrometry. Journal of Agricultural and Food Chemistry. 2017; 65(3): 575-585, doi: 10.1021/acs.jafc.6b04234.
  • Wen, Y, Wang, L, Jin, Y, Zhang, J, Su, L, Zhang, X, Zhou, J, Li, Y. The Microbial Community Dynamics during the Vitex Honey Ripening Process in the Honeycomb. Front Microbiol. 2017; 8: 1649, doi: 10.3389/fmicb.2017.01649.
  • Weston, RJ, Brocklebank, LK. The oligosaccharide composition of some New Zealand honeys. Food Chemistry. 1999; 64(1): 33-37, doi: 10.1016/s0308-8146(98)00099-5.
  • Xiong, ZR, Sogin, JH, Worobo, RW. Microbiome analysis of raw honey reveals important factors influencing the bacterial and fungal communities. Frontiers in Microbiology. 2022; 13: 1099522, doi: 10.3389/fmicb.2022.1099522.
  • Xu, P, Shi, M, Chen, XX. Antimicrobial peptide evolution in the Asiatic honey bee Apis cerana. Plos One. 2009; 4(3)(1): e4239, doi: 10.1371/journal.pone.0004239.
  • Zacharof, MP, Lovitt, RW. "Bacteriocins produced by lactic acid bacteria: A review article." In "APCBEE Procedia (ICBFS 2012: April 7-8, 2012, Bangkok, Thailand)". Vol. 2, 2012. p. 50-56. Print.
  • Zendo, T, Ohashi, C, Maeno, S, Piao, X, Salminen, S, Sonomoto, K, Endo, A, Zhang, YZ, Chen, YF, Wu, YQ, Si, JJ, Zhang, CP, Zheng, HQ, Hu, FL. Kunkecin A, a New Nisin Variant Bacteriocin Produced by the Fructophilic Lactic Acid Bacterium, Apilactobacillus kunkeei FF30-6 Isolated From Honey Bees Discrimination of the entomological origin of honey according to the secretions of the bee (Apis cerana or Apis mellifera). Frontiers in Microbiology. 2020; 11: 571903, doi: 10.3389/fmicb.2020.571903.
  • Zhang, YZ, Chen, YF, Wu, YQ, Si, JJ, Zhang, CP, Zheng, HQ, Hu, FL. Discrimination of the entomological origin of honey according to the secretions of the bee (Apis cerana or Apis mellifera). Food Research International. 2019; 116: 362-369, doi: 10.1016/j.foodres.2018.08.049.
  • Zhao, H, Cheng, N, Zhou, W, Chen, S, Wang, Q, Gao, H, Cao, W. Honey polyphenols ameliorate DSS-induced ulcerative colitis via modulating gut microbiota in rats. Molecular Nutrition & Food Research. 2019; 63(23): e1900638, doi: 10.1002/mnfr.201900638.
  • Zhao, X, Kuipers, OP. Identification and classification of known and putative antimicrobial compounds produced by a wide variety of Bacillales species. BMC Genomics. 2016; 17(1): 882, doi: 10.1186/s12864-016-3214-2.
  • Zheng, YZ, Deng, G, Liang, Q, Chen, DF, Guo, R, Lai, RC. Antioxidant activity of quercetin and its glucosides from propolis: A theoretical study. Scientific Reports. 2017; 7(1): 7543, doi: 10.1038/s41598-017-08024-8.
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Details

Primary Language English
Subjects Field Crops and Pasture Production (Other)
Journal Section Review
Authors

Rustem Ilyasov 0000-0003-2445-4739

Dmitry Boguslavsky This is me 0000-0001-9601-640X

Alla Ilyasova This is me 0000-0002-7505-6805

Vener Sattarov This is me 0000-0001-6331-4398

Valery Danilenko This is me 0000-0001-5780-0621

Project Number 24-16-00179
Early Pub Date November 12, 2024
Publication Date November 18, 2024
Submission Date July 7, 2024
Acceptance Date September 20, 2024
Published in Issue Year 2024 Volume: 24 Issue: 2

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Vancouver Ilyasov R, Boguslavsky D, Ilyasova A, Sattarov V, Danilenko V. A MULTIFACETED BIOACTIVITY OF HONEY: INTERACTIONS BETWEEN BEES, PLANTS AND MICROORGANISMS. U. Arı. D.-U. Bee J. 2024;24(2):356-85.

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