YUAN Wenqin, XUAN Hongzhuan, WANG Kai. Research Progress of the Antibacterial Active Substances from Honey and Their Antibacterial Mechanisms[J]. Science and Technology of Food Industry, 2023, 44(4): 438−446. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2022030349.
Citation: YUAN Wenqin, XUAN Hongzhuan, WANG Kai. Research Progress of the Antibacterial Active Substances from Honey and Their Antibacterial Mechanisms[J]. Science and Technology of Food Industry, 2023, 44(4): 438−446. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2022030349.

Research Progress of the Antibacterial Active Substances from Honey and Their Antibacterial Mechanisms

More Information
  • Received Date: March 28, 2022
  • Available Online: December 14, 2022
  • Honey is a natural sweet substance made from a mixture of nectar collected by worker bees and their own secretions, which has good antibacterial activity and contains a variety of natural antibacterial active substances. In recent years, a large number of studies have been reported on the progress of antimicrobial active substances in honey, including methylglyoxal, hydrogen peroxide, polyphenols, antimicrobial peptides and Major royal jelly proteins. Numerous studies have shown that hydrogen peroxide is one of the most important antibacterial substances in honey. This paper highlights the important roles by each antimicrobial effective active substance for the anti-bacterial by honey. It also further summarizes the process of glucose oxidase catalyzing the production of hydrogen peroxide from glucose. The process of glucose oxidase catalyzing the production of hydrogen peroxide from glucose is summarized using hydrogen peroxide in honey as an example. Other pathways for the production and degradation of hydrogen peroxide and the physicochemical factors affecting the production of hydrogen peroxide are also reviewed. Rational regulation of hydrogen peroxide production in honey plays an important role in its antibacterial and even other biological activities. This review would also provide a reference for the safe clinical use of honey and the development of functional foods.
  • [1]
    郝博, 鹿扩建, 笔雪艳. 蜂蜜作为药用辅料应用及质量控制的研究概述[J]. 中医药学报,2020,48(10):69−74. [HAO B, LU K J, BI X Y. Research overview on applications as pharmaceutical excipient and quality control of honey[J]. Acta Chinese Medicine and Pharmacology,2020,48(10):69−74.
    [2]
    TASHKANDI H. Honey in wound healing: An updated review[J]. Open Life Sci,2021,16(1):1091−100. doi: 10.1515/biol-2021-0084
    [3]
    周帆, 陈碧霄, 杨淼, 等. 蜂蜜中抗菌活性成分研究进展[J]. 现代食品,2020(11):6−7. [ZHOU F, CHEN B X, YANG M, et al. Research progress on antibacterial active ingredients in honey[J]. Modern Food,2020(11):6−7.
    [4]
    SCEPANKOVA H, PINTO C A, PAULA V, et al. Conventional and emergent technologies for honey processing: A perspective on microbiological safety, bioactivity, and quality[J]. Comprehensive Reviews in Food Science and Food Safety,2021,20(6):5393−5420. doi: 10.1111/1541-4337.12848
    [5]
    SERAGLIO S K T, SILVA B, BERGAMO G, et al. An overview of physicochemical characteristics and health-promoting properties of honeydew honey[J]. Food Research International,2019,119:44−66. doi: 10.1016/j.foodres.2019.01.028
    [6]
    HU F L. Chemical analyses and antimicrobial activity of nine kinds of unifloral Chinese honeys compared to Manuka honey (12+and 20+)[J]. Molecules,2021,26(9):2778. doi: 10.3390/molecules26092778
    [7]
    FARKASOVSKA J, BUGAROVA V, GODOCIKOVA J, et al. The role of hydrogen peroxide in the antibacterial activity of different floral honeys[J]. European Food Research and Technology,2019,245(12):2739−2744. doi: 10.1007/s00217-019-03393-y
    [8]
    MCLOONE P, WARNOCK M, FYFE L. Honey: A realistic antimicrobial for disorders of the skin[J]. Journal of Microbiology, Immunology and Infection,2016,49(2):161−167. doi: 10.1016/j.jmii.2015.01.009
    [9]
    BRUDZYNSKI K. Effect of hydrogen peroxide on antibacterial activities of Canadian honeys[J]. Canadian Journal of Microbiology,2006,52(12):1228−1237. doi: 10.1139/w06-086
    [10]
    苏睿, 秦加敏, 董坤, 等. 弗里熊蜂蜜罐中糖液成分分析[J]. 昆虫学报,2021,64(1):90−98. [SU R, QIN J M, DONG K, et al. Component analysis of the sugar solution stored in wax cells by Bombus friseanus (Hymenoptera: Apidae)[J]. Acta Entomologica Sinica,2021,64(1):90−98.
    [11]
    汪思凡, 曹振辉, 潘洪彬, 等. 蜂蜜化学成分及其主要生物学功能研究进展[J]. 食品研究与开发,2018,39(1):176−181. [WANG S F, CAO Z H, PAN H B, et al. Research progress on chemical composition and major biological function of honey[J]. Food Research and Development,2018,39(1):176−181.
    [12]
    郭娜娜, 赵亚周, 王凯, 等. 蜂蜜对创伤愈合的作用及临床治疗研究进展[J]. 中国农业科技导报,2021,23(2):123−133. [GUO N N, ZHAO Y Z, WANG K, et al. Research progress on the effects of honey on wound healing and its mechanism[J]. Journal of Agricultural Science and Technology,2021,23(2):123−133.
    [13]
    张飞龙. 米林县不同蜜源蜂蜜抗菌活性和过氧化氢含量的测定[J]. 食品安全导刊,2021(12):116−118. [ZHANG F L. Determination of antibacterial activity and hydrogen peroxide content of honey from different sources in Millin County[J]. China Food Safety Magazine,2021(12):116−118.
    [14]
    吴雨祺, 郑宇斐, 张言政, 等. 蜂蜜中抗菌活性物质的研究进展[J]. 中国蜂业,2017,68(1):17−20. [WU Y Q, ZHENG Y F, ZHANG Y Z, et al. Research progress on antibacterial substances in honey[J]. Apiculture of China,2017,68(1):17−20.
    [15]
    MAJTAN J, BUCEKOVA M, KAFANTARIS I, et al. Honey antibacterial activity: A neglected aspect of honey quality assurance as functional food[J]. Trends in Food Science & Technology,2021,118:870−886.
    [16]
    张言政, 胡福良. 麦卢卡蜂蜜的抗菌活性及其机理[J]. 蜜蜂杂志,2015,35(7):1−5. [ZHANG Y Z, HU F L. Antibacterial activity of Manuka honey and its mechanism[J]. Journal of Bee,2015,35(7):1−5.
    [17]
    JOHNSTON M, MCBRIDE M, DAHIYA D, et al. Antibacterial activity of Manuka honey and its components: An overview[J]. AIMS Microbiology,2018,4(4):655−664. doi: 10.3934/microbiol.2018.4.655
    [18]
    王玉涵, 王欣然, 李熠, 等. 蜂蜜中功能营养成分及特征研究进展[J]. 农产品质量与安全,2020(4):85−92. [WANG Y H, WANG X R, LI Y, et al. Research progress on functional nutrition components and characteristics of honey[J]. Quality and Safety of Agro-Products,2020(4):85−92.
    [19]
    杨二林, 赵浩安, 徐元元, 等. 枣花蜜酚类化合物组成及其抗氧化活性分析[J]. 食品科学,2021,42(3):150−157. [YANG E L, ZHAO H A, XU Y Y, et al. Phenolic compounds and antioxidant activity of jujube honey[J]. Food Science,2021,42(3):150−157. doi: 10.7506/spkx1002-6630-20200221-227
    [20]
    王笑笑, 周勇, 徐国群, 等. 黄酮类成分在蜂蜜抗菌性中的效能研究[J]. 中国现代应用药学,2017,34(3):363−369. [WANG X X, ZHOU Y, XU G Q, et al. Study on the efficacy of flavonoids in the antibacterial properties of honey[J]. Chinese Journal of Modern Applied Pharmacy,2017,34(3):363−369.
    [21]
    阚玉红, 谢笔钧, 孙智达. 胭脂红番石榴叶黄酮提取物的抑菌活性及其机理[J]. 中国调味品,2021,46(12):159−166, 188. [KAN Y H, XIE B D, SUN Z D. Antibacterial activity and mechanism of flavonoids extracted from leaves of Psidium guajava L[J]. China Condiment,2021,46(12):159−166, 188. doi: 10.3969/j.issn.1000-9973.2021.12.030
    [22]
    ZHANG G, YANG Y, MEMON F U, et al. A natural antimicrobial agent: Analysis of antibacterial effect and mechanism of compound phenolic acid on Escherichia coli based on tandem mass tag proteomics[J]. Frontiers in Microbiology,2021,12:738896. doi: 10.3389/fmicb.2021.738896
    [23]
    DA SILVA P M, GAUCHE C, GONZAGA L V, et al. Honey: Chemical composition, stability and authenticity[J]. Food Chemistry,2016,196:309−323. doi: 10.1016/j.foodchem.2015.09.051
    [24]
    张爱静, 张爱提, 陈俊丽, 等. 中华蜜蜂防御素基因克隆及生物信息学分析[J]. 特产研究,2011,33(2):13−16. [ZHANG A J, ZHANG A T, CHEN J L, et al. Gene clone and bioinformatics analysis of bee defensins[J]. Special Wild Economic Animal and Plant Research,2011,33(2):13−16. doi: 10.3969/j.issn.1001-4721.2011.02.004
    [25]
    HELBING S, LATTORFF H M G, MORITZ R F A, et al. Comparative analyses of the major royal jelly protein gene cluster in three Apis species with long amplicon sequencing[J]. DNA Research,2017,24(3):279−287. doi: 10.1093/dnares/dsw064
    [26]
    KATRINA B, CALVIN S, ROBERT L. MRJP1-containing glycoproteins isolated from honey, a novel antibacterial drug candidate with broad spectrum activity against multi-drug resistant clinical isolates[J]. Frontiers in Microbiology,2015(6):711.
    [27]
    FENG M, FANG Y, MA C, et al. Mechanistic insight into royal protein inhibiting the gram-positive bacteria[J]. Biomolecules,2021,11(1):64. doi: 10.3390/biom11010064
    [28]
    伊作林, 杨柳, 席芳贵, 等. 蜂蜜成分及功能活性的研究进展[J]. 中国养蜂,2018,69(4):51−54. [YI Z L, YANG L, XI F G, et al. Advances in the study of components and functional activities of honey[J]. Apiculture of China,2018,69(4):51−54.
    [29]
    张国志, 张言政, 李珊珊, 等. 蜂蜜中的酶及其在蜂蜜质量控制中的应用[J]. 食品安全质量检测学报,2021,12(21):8313−8320. [ZHANG G Z, ZHANG Y Z, LI S S, et al. Enzymes in honey and their application in honey quality control[J]. Journal of Food Safety & Quality,2021,12(21):8313−8320. doi: 10.3969/j.issn.2095-0381.2021.21.spaqzljcjs202121002
    [30]
    WOHLFAHRT G, WITT S, HENDLE J, et al. 1.8 and 1.9 A resolution structures of the Penicillium amagasakiense and Aspergillus niger glucose oxidases as a basis for modelling substrate complexes[J]. Acta Crystallographica Section D Biological Crystallography, 1999, 55(Pt 5): 969-977.
    [31]
    LESKOVAC V, TRIVIC S, WOHLFAHRT G, et al. Glucose oxidase from Aspergillus niger: The mechanism of action with molecular oxygen, quinones, and one-electron acceptors[J]. International Journal of Biochemistry and Cell Biology,2005,37(4):731−750. doi: 10.1016/j.biocel.2004.10.014
    [32]
    GIBSON Q H, SWOBODA B E, MASSEY V. Kinetics and mechanism of action of glucose oxidase[J]. J Biol Chem,1964,239:3927−3934. doi: 10.1016/S0021-9258(18)91224-X
    [33]
    BRUDZYNSKI K. A current perspective on hydrogen peroxide production in honey. A review[J]. Food Chemistry,2020,332:127229. doi: 10.1016/j.foodchem.2020.127229
    [34]
    SCHEPARTZ A I, SUBERS M H. The glucose oxidase of honey I. Purification and some general properties of the enzyme[J]. Biochimica et Biophysica Acta (BBA)-Specialized Section on Enzymological Subjects,1964,85(2):228−237. doi: 10.1016/0926-6569(64)90243-3
    [35]
    ABRAMOVI H, JAMNIK M, BURKAN L, et al. Water activity and water content in Slovenian honeys[J]. Food Control,2008,19(11):1086−1090. doi: 10.1016/j.foodcont.2007.11.008
    [36]
    KALISZ H M, HENDLE J, SCHMID R D. Structural and biochemical properties of glycosylated and deglycosylated glucose oxidase from Penicillium amagasakiense[J]. Applied Microbiology and Biotechnology,1997,47(5):502−507. doi: 10.1007/s002530050963
    [37]
    STRELEC, IVICA, CREVAR, et al. Glucose oxidase activity and hydrogen peroxide accumulation in Croatian honeys[J]. Croatian Journal of Food Science and Technology,2018,10(1):33−41. doi: 10.17508/CJFST.2018.10.1.06
    [38]
    NAKAMURA S, OGURA Y. Mode of inhibition of glucose oxidase by metal ions[J]. Journal of Biochemistry,1968,64(4):439. doi: 10.1093/oxfordjournals.jbchem.a128915
    [39]
    TOMOTANI E J, NEVES L, VITOLO M. Oxidation of glucose to gluconic acid by glucose oxidase in a membrane bioreactor[J]. Applied Biochemistry & Biotechnology Part A Enzyme Engineering & Biotechnology,2005,124(1−3):149−162.
    [40]
    JIE B, FURUMOTO K, YOSHIMOTO M, et al. Competitive inhibition by hydrogen peroxide produced in glucose oxidation catalyzed by glucose oxidase[J]. Biochemical Engineering Journal,2003,13(1):69−72. doi: 10.1016/S1369-703X(02)00120-1
    [41]
    BRUDZYNSKI K, MIOTTO D, KIM L, et al. Active macromolecules of honey form colloidal particles essential for honey antibacterial activity and hydrogen peroxide production[J]. Scientific Reports,2017,7(1):7637. doi: 10.1038/s41598-017-08072-0
    [42]
    BANG L M, BUNTTING C, MOLAN P. The effect of dilution on the rate of hydrogen peroxide production in honey and its implications for wound healing[J]. J Altern Complement Med,2003,9(2):267−273. doi: 10.1089/10755530360623383
    [43]
    WHITE J W, SUBERS M H, SCHEPARTZ A I. The identification of inhibine, the antibacterial factor in honey, as hydrogen peroxide and its origin in a honey glucose-oxidase system[J]. Biochim Biophys Acta,1963,73(1):57−70. doi: 10.1016/0926-6569(63)90108-1
    [44]
    SCHEPARTZ A I. The glucose oxidase of honey. IV. Some addition observations[J]. Biochimica et Biophysica Acta (BBA)-Enzymology and Biological Oxidation, 1966, 118(3): 637-640.
    [45]
    DUSTMANN J H. Über die katalaseaktivität in bienenhonig aus der tracht der heidekrautgewächse (Ericaceae)[J]. Zeitschrift für Lebensmittel-Untersuchung und Forschung,1971,145(5):294−295.
    [46]
    ZáMOCKY M, GASSELHUBER B, FURTMüLLER P, et al. Molecular evolution of hydrogen peroxide degrading enzymes[J]. Archives of Biochemistry and Biophysics,2012,525(2):131−144. doi: 10.1016/j.abb.2012.01.017
    [47]
    樊永华, 许辉. 蜂蜜的营养及药用价值[J]. 科技经济市场,2015(10):113−114. [FAN Y H, XU H. Nutrition and medicinal value of honey[J]. Science & Technology Ecnony Market,2015(10):113−114. doi: 10.3969/j.issn.1009-3788.2015.10.086
    [48]
    KERKVLIET D J. Screening method for the determination of peroxide acumulation in honey and relation with HMF content[J]. Journal of Apicultural Research,1996,35(3-4):110−117. doi: 10.1080/00218839.1996.11100920
    [49]
    ALSCHER R G, HESS J L. Antioxidants in higher plants[M]. CRC Press, 1993.
    [50]
    AKAGAWA M, SHIGEMITSU T, SUYAMA K. Production of hydrogen peroxide by polyphenols and polyphenol-rich beverages under quasi-physiological conditions[J]. Bioscience, Biotechnology, and Biochemistry,2003,67(12):2632−2640. doi: 10.1271/bbb.67.2632
    [51]
    ATANASOVA V, FULCRAND H, CHEYNIER V, et al. Effect of oxygenation on polyphenol changes occurring in the course of wine-making[J]. Analytica Chimica Acta,2002,458(1):15−27. doi: 10.1016/S0003-2670(01)01617-8
    [52]
    GRZESIK M, BARTOSZ G, STEFANIUK I, et al. Dietary antioxidants as a source of hydrogen peroxide[J]. Food Chemistry,2019,278:692−699. doi: 10.1016/j.foodchem.2018.11.109
    [53]
    FUKUMOTO L, MAZZA G. Assessing antioxidant and prooxidant activities of phenolic compounds[J]. Journal of Agricultural and Food Chemistry,2000,48(8):3597−3604. doi: 10.1021/jf000220w
    [54]
    CAO G, SOFIC E, PRIOR R L. Antioxidant and prooxidant behavior of flavonoids: Structure-activity relationships[J]. Free Radic Biol Med,1997,22(5):749−760. doi: 10.1016/S0891-5849(96)00351-6
    [55]
    BERTONCELJ J, DOBERSEK U, JAMNIK M, et al. Evaluation of the phenolic content, antioxidant activity and colour of Slovenian honey[J]. Food Chemistry,2007,105(2):822−828. doi: 10.1016/j.foodchem.2007.01.060
    [56]
    ESTEVINHO L, PEREIRA A P, MOREIRA L, et al. Antioxidant and antimicrobial effects of phenolic compounds extracts of Northeast Portugal honey[J]. Food and Chemical Toxicology,2008,46(12):3774−3779. doi: 10.1016/j.fct.2008.09.062
    [57]
    VELA L, DE LORENZO C, PéREZ R A. Antioxidant capacity of Spanish honeys and its correlation with polyphenol content and other physicochemical properties[J]. Journal of the Science of Food and Agriculture,2007,87(6):1069−1075. doi: 10.1002/jsfa.2813
    [58]
    BRUDZYNSKI K, ABUBAKER K, WANG T. Powerful bacterial killing by buckwheat honeys is concentration-dependent, involves complete DNA degradation and requires hydrogen peroxide[J]. Frontiers in Microbiology,2012,3:242.
    [59]
    BRUDZYNSKI K, LANNIGAN R. Mechanism of honey bacteriostatic action against MRSA and VRE involves hydroxyl radicals generated from honey's hydrogen peroxide[J]. Frontiers in Microbiology,2012,3:36.
    [60]
    BUCEKOVA M, BURIOVA M, PEKARIK L, et al. Phytochemicals-mediated production of hydrogen peroxide is crucial for high antibacterial activity of honeydew honey[J]. Scientific Reports,2018,8(1):1−9.
    [61]
    BRUDZYNSKI K, ABUBAKER K, MIOTTO D. Unraveling a mechanism of honey antibacterial action: Polyphenol/H2O2-induced oxidative effect on bacterial cell growth and on DNA degradation[J]. Food Chemistry,2012,133(2):329−336. doi: 10.1016/j.foodchem.2012.01.035
    [62]
    黎俏文, 秦俊豪, 陈桂葵, 等. H2O2介导的Fenton反应对砷镉污染下水稻生物量的影响[J]. 农业环境科学学报,2015,34(7):1233−1238. [LI Q W, QIN J H, CHEN G K, et al. Effect of hydrogen peroxide induced Fenton Reaction on biomass of rice in soil contaminated by Cd and As[J]. Journal of Agro-Environment Science,2015,34(7):1233−1238.
    [63]
    HARPER A D, STALNAKER S H, WELLS L, et al. Interaction of nectarin 4 with a fungal protein triggers a microbial surveillance and defense mechanism in nectar[J]. Phytochemistry,2010,71(17-18):1963−1969. doi: 10.1016/j.phytochem.2010.09.009
    [64]
    KAČÁNIOVÁ M, KŇAZOVICKÁ V, FELŠÖCIOVÁ S, et al. Microscopic fungi recovered from honey and their toxinogenity[J]. Journal of Environmental Science and Health, Part A,2012,47(11):1659−1664. doi: 10.1080/10934529.2012.687242
    [65]
    BRUDZYNSKI K. Honey as an ecological reservoir of antibacterial compounds produced by antagonistic microbial interactions in plant nectars, honey and honey bee[J]. Antibiotics,2021,10(5):551.
    [66]
    BRUDZYNSKI K, SJAARDA C P. Colloidal structure of honey and its influence on antibacterial activity[J]. Compr Rev Food Sci Food Saf,2021,20(2):2063−2080. doi: 10.1111/1541-4337.12720
    [67]
    JOHNSON B J, ALGAR W R, MALANOSKI A P, et al. Understanding enzymatic acceleration at nanoparticle interfaces: Approaches and challenges[J]. Nano Today,2014,9(1):102−131. doi: 10.1016/j.nantod.2014.02.005
  • Cited by

    Periodical cited type(3)

    1. 陈家伟,谈婷,丁丽,王星,肖理文. 黄曲霉毒素B_1/呕吐毒素/玉米赤霉烯酮三合一时间分辨荧光定量快速检测卡的样品稀释液优化. 粮食加工. 2025(02): 114-119+131 .
    2. 韩冰,贾永梅,李志果,周国华,刘培炼,余彪,张玲玲,薛茗月. 核酸适配体传感器在黄曲霉毒素B1检测中应用研究进展. 分析科学学报. 2022(03): 371-376 .
    3. 王哲,陈芳,董丽,胡小松. 表面增强拉曼光谱在食源性致病菌检测中的应用研究进展. 食品研究与开发. 2022(17): 184-193 .

    Other cited types(6)

Catalog

    Article Metrics

    Article views (495) PDF downloads (47) Cited by(9)

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return