Research progress in temporospatial characteristics and functions of gut microbiota in honeybees
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Affiliation:

1.Honeybee Research Institute, Jiangxi Agricultural University, Nanchang, Jiangxi, China;2.Jiangxi Province Key Laboratory of Honeybee Biology and Beekeeping, Nanchang, Jiangxi, China;3.Institute of Surveillance and Prevention of Animal Group Diseases, Jiangxi Agricultural University, Nanchang, Jiangxi, China;4.Jiangxi Provincial Key Laboratory for Animal Health, Nanchang, Jiangxi, China

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This work was supported by the National Natural Science Foundation of China (32372942).

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    Abstract:

    Honeybees (Apis mellifera) are important pollinators worldwide and models for the research on development and behaviors, showcasing great economic, environmental, and scientific benefits. As the symbiont of honeybees, the gut microbiota is transmitted through social behavioral interactions and plays a crucial role in the development and health of honeybees. It not only helps honeybees digest and absorb nutrients but also helps resist pathogen invasion and enhance immunity. Recently, honeybees have emerged as the models for studying gut microbiota. Researchers not only analyzed the composition and function of the gut microbiota in honeybees but also explored the diversity and functions of strains. This paper reviews the temporospatial dynamics of the gut microbiota in honeybees, the factors affecting the gut microbiota, the influences of the gut microbiota on the biological characteristics and health of honeybees, and the functional applications of the gut microbiota, providing references for the research and application of the gut microbiota in honeybees.

    Reference
    [1] LIU JH, LIAO CH, LI Z, SHI XX, WU XB. Synergistic resistance of honeybee (Apis mellifera) and their gut microorganisms to fluvalinate stress[J]. Pesticide Biochemistry and Physiology, 2024, 201: 105865.
    [2] GOULSON D, NICHOLLS E, BOTíAS C, ROTHERAY EL. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers[J]. Science, 2015, 347(6229): 1255957.
    [3] SHI JL, YANG HY, YU LT, LIAO CH, LIU Y, JIN MJ, YAN WY, WU XB. Sublethal acetamiprid doses negatively affect the lifespans and foraging behaviors of honey bee (Apis mellifera L.) workers[J]. Science of the Total Environment, 2020, 738: 139924.
    [4] 李家豪, 冯启理, 韩日畴. 蜜蜂肠道微生物研究进展[J]. 环境昆虫学报, 2020, 42(6): 1369-1382.LI JH, FENG QL, HAN RC. Gut microbiota of honey bees[J]. Journal of Environmental Entomology, 2020, 42(6): 1369-1382 (in Chinese).
    [5] MOTTA EVS, MORAN NA. The honeybee microbiota and its impact on health and disease[J]. Nature Reviews Microbiology, 2024, 22(3): 122-137.
    [6] LIU JH, SHI JL, HU YY, SU YC, ZHANG YH, WU XB. Flumethrin exposure perturbs gut microbiota structure and intestinal metabolism in honeybees (Apis mellifera)[J]. Journal of Hazardous Materials, 2024, 480: 135886.
    [7] Luo SQ, Zhang X, Zhou X. Temporospatial dynamics and host specificity of honeybee gut bacteria[J]. Cell Reports, 2024, 43(7): 114408.
    [8] ZHENG JS, WITTOUCK S, SALVETTI E, FRANZ CMAP, HARRIS HMB, MATTARELLI P, O’TOOLE PW, POT B, VANDAMME P, WALTER J, WATANABE K, WUYTS S, FELIS GE, G?NZLE MG, LEBEER S. A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae[J]. International Journal of Systematic and Evolutionary Microbiology, 2020, 70(4): 2782-2858.
    [9] KWONG WK, MORAN NA. Gut microbial communities of social bees[J]. Nature Reviews Microbiology, 2016, 14(6): 374-384.
    [10] MARTINSON VG, MOY J, MORAN NA. Establishment of characteristic gut bacteria during development of the honeybee worker[J]. Applied and Environmental Microbiology, 2012, 78(8): 2830-2840.
    [11] 郭军, 李继莲, 吴杰. 蜜蜂个体发育过程中特定肠道菌的形成[J]. 中国蜂业, 2015, 65(2): 62-65.GUO J, LI JL, WU J. Formation of specific intestinal bacteria during the ontogenesis of honeybees[J]. Apiculture of China, 2015, 65(2): 62-65 (in Chinese).
    [12] KHAN KA, GANESHPRASAD DN, SACHIN HR, SHOUCHE YS, GHRAMH HA, SNEHARANI AH. Gut microbial diversity in Apis cerana indica and Apis florea colonies: a comparative study[J]. Frontiers in Veterinary Science, 2023, 10: 1149876.
    [13] HRONCOVA Z, KILLER J, HAKL J, TITERA D, HAVLIK J. In-hive variation of the gut microbial composition of honey bee larvae and pupae from the same oviposition time[J]. BMC Microbiology, 2019, 19(1): 110.
    [14] HRONCOVA Z, HAVLIK J, KILLER J, DOSKOCIL I, TYL J, KAMLER M, TITERA D, HAKL J, MRAZEK J, BUNESOVA V, RADA V. Variation in honey bee gut microbial diversity affected by ontogenetic stage, age and geographic location[J]. PLoS One, 2015, 10(3): e0118707.
    [15] ELIJAH POWELL J, MARTINSON VG, URBAN-MEAD K, MORAN NA. Routes of acquisition of the gut microbiota of the honey bee Apis mellifera[J]. Applied and Environmental Microbiology, 2014, 80(23): 7378-7387.
    [16] KWONG WK, ENGEL P, KOCH H, MORAN NA. Genomics and host specialization of honey bee and bumble bee gut symbionts[J]. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(31): 11509-11514.
    [17] SMITH EA, ANDERSON KE, CORBY-HARRIS V, McFREDERICK QS, PARISH AJ, RICE DW, NEWTON ILG. Reclassification of seven honey bee symbiont strains as Bombella apis[J]. International Journal of Systematic and Evolutionary Microbiology, 2021. DOI: 10.1099/ijsem.0.004950.
    [18] TARPY DR, MATTILA HR, NEWTON ILG. Development of the honey bee gut microbiome throughout the queen-rearing process[J]. Applied and Environmental Microbiology, 2015, 81(9): 3182-3191.
    [19] ELIJAH POWELL J, EIRI DR, MORAN NA, RANGEL J. Modulation of the honey bee queen microbiota: effects of early social contact[J]. PLoS One, 2018, 13(7): e0200527.
    [20] KAPHEIM KM, RAO VD, YEOMAN CJ, WILSON BA, WHITE BA, GOLDENFELD N, ROBINSON GE. Caste-specific differences in hindgut microbial communities of honey bees (Apis mellifera)[J]. PLoS One, 2015, 10(4): e0123911.
    [21] ANDERSON KE, RICIGLIANO VA, COPELAND DC, MOTT BM, MAES P. Social interaction is unnecessary for hindgut microbiome transmission in honey bees: the effect of diet and social exposure on tissue-specific microbiome assembly[J]. Microbial Ecology, 2023, 85(4): 1498-1513.
    [22] ANDERSON KE, RICIGLIANO VA, MOTT BM, COPELAND DC, FLOYD AS, MAES P. The queen’s gut refines with age: longevity phenotypes in a social insect model[J]. Microbiome, 2018, 6(1): 108.
    [23] VERNIER CL, NGUYEN LA, GERNAT T, AHMED AC, CHEN ZQ, ROBINSON GE. Gut microbiota contribute to variations in honey bee foraging intensity[J]. The ISME Journal, 2024, 18(1): wrae030.
    [24] LIBERTI J, FRANK ET, KAY T, KESNER L, MONIé-IBANES M, QUINN A, SCHMITT T, KELLER L, ENGEL P. Gut microbiota influences onset of foraging-related behavior but not physiological hallmarks of division of labor in honeybees[J]. mBio, 2024, 15(9): e0103424.
    [25] BAUD GLC, PRASAD A, ELLEGAARD KM, ENGEL P. Turnover of strain-level diversity modulates functional traits in the honeybee gut microbiome between nurses and foragers[J]. Genome Biology, 2023, 24(1): 283.
    [26] KE?NEROVá L, EMERY O, TROILO M, LIBERTI J, ERKOSAR B, ENGEL P. Gut microbiota structure differs between honeybees in winter and summer[J]. The ISME Journal, 2020, 14(3): 801-814.
    [27] JONES JC, FRUCIANO C, MARCHANT J, HILDEBRAND F, FORSLUND S, BORK P, ENGEL P, HUGHES WH. The gut microbiome is associated with behavioural task in honey bees[J]. Insectes Sociaux, 2018, 65(3): 419-429.
    [28] GRUNECK L, GENTEKAKI E, KHONGPHINITBUNJONG K, POPLUECHAI S. Distinct gut microbiota profiles of Asian honey bee (Apis cerana) foragers[J]. Archives of Microbiology, 2022, 204(3): 187.
    [29] MINDY NELSON C, IHLE KE, KIM FONDRK M, PAGE RE, AMDAM GV. The gene vitellogenin has multiple coordinating effects on social organization[J]. PLoS Biology, 2007, 5(3): e62.
    [30] CORBY-HARRIS V, MAES P, ANDERSON KE. The bacterial communities associated with honey bee (Apis mellifera) foragers[J]. PLoS One, 2014, 9(4): e95056.
    [31] ENGEL P, BARTLETT KD, MORAN NA. The bacterium Frischella perrara causes scab formation in the gut of its honeybee host[J]. mBio, 2015, 6(3): e00193-15.
    [32] FLINT HJ, DUNCAN SH, LOUIS P. The impact of nutrition on intestinal bacterial communities[J]. Current Opinion in Microbiology, 2017, 38: 59-65.
    [33] KWONG WK, MEDINA LA, KOCH H, SING KW, SOH EJY, ASCHER JS, JAFFé R, MORAN NA. Dynamic microbiome evolution in social bees[J]. Science Advances, 2017, 3(3): e1600513.
    [34] WU YQ, ZHENG YF, WANG S, CHEN YP, TAO JY, CHEN YN, CHEN GW, ZHAO HX, WANG K, DONG K, HU FL, FENG Y, ZHENG HQ. Genetic divergence and functional convergence of gut bacteria between the eastern honey bee Apis cerana and the western honey bee Apis mellifera[J]. Journal of Advanced Research, 2022, 37: 19-31.
    [35] MATTILA HR, RIOS D, WALKER-SPERLING VE, ROESELERS G, NEWTON ILG. Characterization of the active microbiotas associated with honey bees reveals healthier and broader communities when colonies are genetically diverse[J]. PLoS One, 2012, 7(3): e32962.
    [36] BRIDSON C, VELLANIPARAMBIL L, ANTWIS RE, MüLLER W, TUCKER GILMAN R, ROWNTREE JK. Genetic diversity of honeybee colonies predicts gut bacterial diversity of individual colony members[J]. Environmental Microbiology, 2022, 24(12): 5643-5653.
    [37] SU QZ, TANG M, HU JH, TANG JB, ZHANG X, LI XG, NIU QS, ZHOU XG, LUO SQ, ZHOU X. Significant compositional and functional variation reveals the patterns of gut microbiota evolution among the widespread Asian honeybee populations[J]. Frontiers in Microbiology, 2022, 13: 934459.
    [38] WRIGHT GA, NICOLSON SW, SHAFIR S. Nutritional physiology and ecology of honey bees[J]. Annual Review of Entomology, 2018, 63: 327-344.
    [39] ZHENG H, PERREAU J, ELIJAH POWELL J, HAN BF, ZHANG ZJ, KWONG WK, TRINGE SG, MORAN NA. Division of labor in honey bee gut microbiota for plant polysaccharide digestion[J]. Proceedings of the National Academy of Sciences of the United States of America, 2019, 116(51): 25909-25916.
    [40] RICIGLIANO VA, FITZ W, COPELAND DC, MOTT BM, MAES P, FLOYD AS, DOCKSTADER A, ANDERSON KE. The impact of pollen consumption on honey bee (Apis mellifera) digestive physiology and carbohydrate metabolism[J]. Archives of Insect Biochemistry and Physiology, 2017. DOI: 10.1002/arch.21406.
    [41] RICIGLIANO VA, ANDERSON KE. Probing the honey bee diet-microbiota-host axis using pollen restriction and organic acid feeding[J]. Insects, 2020, 11(5): 291.
    [42] CASTELLI L, BRANCHICCELA B, GARRIDO M, INVERNIZZI C, PORRINI M, ROMERO H, SANTOS E, ZUNINO P, ANTúNEZ K. Impact of nutritional stress on honeybee gut microbiota, immunity, and Nosema ceranae infection[J]. Microbial Ecology, 2020, 80(4): 908-919.
    [43] MAES PW, RODRIGUES PAP, OLIVER R, MOTT BM, ANDERSON KE. Diet-related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honeybee (Apis mellifera)[J]. Molecular Ecology, 2016, 25(21): 5439-5450.
    [44] POWELL JE, LAU P, RANGEL J, ARNOTT R, JONG TD, MORAN NA. The microbiome and gene expression of honey bee workers are affected by a diet containing pollen substitutes[J]. PLoS One, 2023, 18(5): e0286070.
    [45] TAYLOR MA, ROBERTSON AW, BIGGS PJ, RICHARDS KK, JONES DF, PARKAR SG. The effect of carbohydrate sources: sucrose, invert sugar and components of mānuka honey, on core bacteria in the digestive tract of adult honey bees (Apis mellifera)[J]. PLoS One, 2019, 14(12): e0225845.
    [46] HU YY, LIU JH, PAN QZ, SHI XX, WU XB. Effects of artificial sugar supplementation on the composition and nutritional potency of honey from Apis cerana[J]. Insects, 2024, 15(5): 344.
    [47] GUO J, WU J, CHEN YP, EVANS JD, DAI RG, LUO WH, LI JL. Characterization of gut bacteria at different developmental stages of Asian honey bees, Apis cerana[J]. Journal of Invertebrate Pathology, 2015, 127: 110-114.
    [48] ERBAN T, LEDVINKA O, KAMLER M, HORTOVA B, NESVORNA M, TYL J, TITERA D, MARKOVIC M, HUBERT J. Bacterial community associated with worker honeybees (Apis mellifera) affected by European foulbrood[J]. PeerJ, 2017, 5: e3816.
    [49] TRAYNOR KS, MONDET F, de MIRANDA JR, TECHER M, KOWALLIK V, ODDIE MAY, CHANTAWANNAKUL P, McAFEE A. Varroa destructor: a complex parasite, crippling honey bees worldwide[J]. Trends in Parasitology, 2020, 36(7): 592-606.
    [50] HUBERT J, BICIANOVA M, LEDVINKA O, KAMLER M, LESTER PJ, NESVORNA M, KOPECKY J, ERBAN T. Changes in the bacteriome of honey bees associated with the parasite Varroa destructor, and pathogens Nosema and Lotmaria passim[J]. Microbial Ecology, 2017, 73(3): 685-698.
    [51] RUBANOV A, RUSSELL KA, ROTHMAN JA, NIEH JC, McFREDERICK QS. Intensity of Nosema ceranae infection is associated with specific honey bee gut bacteria and weakly associated with gut microbiome structure[J]. Scientific Reports, 2019, 9(1): 3820.
    [52] JABAL-URIEL C, ALBA C, HIGES M, RODRíGUEZ JM, MARTíN-HERNáNDEZ R. Effect of Nosema ceranae infection and season on the gut bacteriome composition of the European honeybee (Apis mellifera)[J]. Scientific Reports, 2022, 12(1): 9326.
    [53] COLIN T, MEIKLE WG, WU XB, BARRON AB. Traces of a neonicotinoid induce precocious foraging and reduce foraging performance in honey bees[J]. Environmental Science & Technology, 2019, 53(14): 8252-8261.
    [54] WU XB, LI Z, YANG HY, HE XJ, YAN WY, ZENG ZJ. The adverse impact on lifespan, immunity, and forage behavior of worker bees (Apis mellifera Linnaeus 1758) after exposure to flumethrin[J]. Science of the Total Environment, 2023, 858: 160146.
    [55] WU XB, LIAO CH, HE XJ, ZHANG LZ, YAN WY, ZENG ZJ. Sublethal fluvalinate negatively affect the development and flight capacity of honeybee (Apis mellifera L.) workers[J]. Environmental Research, 2022, 203: 111836.
    [56] RIBIèRE C, HEGARTY C, STEPHENSON H, WHELAN P, O’TOOLE PW. Gut and whole-body microbiota of the honey bee separate thriving and non-thriving hives[J]. Microbial Ecology, 2019, 78(1): 195-205.
    [57] FERNANDES KE, STANFIELD B, FROST EA, SHANAHAN ER, SUSANTIO D, DONG AZ, TRAN TD, COKCETIN NN, CARTER DA. Low levels of hive stress are associated with decreased honey activity and changes to the gut microbiome of resident honey bees[J]. Microbiology Spectrum, 2023, 11(4): e0074223.
    [58] DAISLEY BA, CHMIEL JA, PITEK AP, THOMPSON GJ, REID G. Missing microbes in bees: how systematic depletion of key symbionts erodes immunity[J]. Trends in Microbiology, 2020, 28(12): 1010-1021.
    [59] HOTCHKISS MZ, POULAIN AJ, FORREST JRK. Pesticide-induced disturbances of bee gut microbiotas[J]. FEMS Microbiology Reviews, 2022, 46(2): fuab056.
    [60] CUESTA-MATé A, RENELIES-HAMILTON J, KRYGER P, JENSEN AB, SINOTTE VM, POULSEN M. Resistance and vulnerability of honeybee (Apis mellifera) gut bacteria to commonly used pesticides[J]. Frontiers in Microbiology, 2021, 12: 717990.
    [61] NAGGAR Y AL, SINGAVARAPU B, PAXTON RJ, WUBET T. Bees under interactive stressors: the novel insecticides flupyradifurone and sulfoxaflor along with the fungicide azoxystrobin disrupt the gut microbiota of honey bees and increase opportunistic bacterial pathogens[J]. Science of the Total Environment, 2022, 849: 157941.
    [62] ZHANG YH, LIU JH, SHI JL, WU BH, HE ZT, WU XB. The interaction and response of gut microbes to exposure to chiral ethiprole in honeybees (Apis mellifera)[J]. Journal of Hazardous Materials, 2025, 486: 137112.
    [63] YU LT, YANG HY, CHENG FP, WU ZH, HUANG Q, HE XJ, YAN WY, ZHANG LZ, WU XB. Honey bee Apis mellifera larvae gut microbial and immune, detoxication responses towards flumethrin stress[J]. Environmental Pollution, 2021, 290: 118107.
    [64] SHI JL, ZHANG RN, PEI YL, LIAO CH, WU XB. Exposure to acetamiprid influences the development and survival ability of worker bees (Apis mellifera L.) from larvae to adults[J]. Environmental Pollution, 2020, 266: 115345.
    [65] RAYMANN K, SHAFFER Z, MORAN NA. Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees[J]. PLoS Biology, 2017, 15(3): e2001861.
    [66] ZHANG ZJ, MU XH, CAO QN, SHI Y, HU XS, ZHENG H. Honeybee gut Lactobacillus modulates host learning and memory behaviors via regulating tryptophan metabolism[J]. Nature Communications, 2022, 13(1): 2037.
    [67] JIA S, WU YQ, CHEN GW, WANG S, HU FL, ZHENG HQ. The pass-on effect of tetracycline-induced honey bee (Apis mellifera) gut community dysbiosis[J]. Frontiers in Microbiology, 2022, 12: 781746.
    [68] TIAN BY, FADHIL NH, ELIJAH POWELL J, KWONG WK, MORAN NA. Long-term exposure to antibiotics has caused accumulation of resistance determinants in the gut microbiota of honeybees[J]. mBio, 2012, 3(6): e00377-12.
    [69] LUDVIGSEN J, PORCELLATO D, L’ABéE-LUND TM, AMDAM GV, RUDI K. Geographically widespread honeybee-gut symbiont subgroups show locally distinct antibiotic-resistant patterns[J]. Molecular Ecology, 2017, 26(23): 6590-6607.
    [70] SUN HH, MU XH, ZHANG KX, LANG HY, SU QZ, LI XG, ZHOU X, ZHANG X, ZHENG H. Geographical resistome profiling in the honeybee microbiome reveals resistance gene transfer conferred by mobilizable plasmids[J]. Microbiome, 2022, 10(1): 69.
    [71] WANG KW, ZHU LY, RAO L, ZHAO L, WANG YT, WU XM, ZHENG H, LIAO XJ. Nano- and micro-polystyrene plastics disturb gut microbiota and intestinal immune system in honeybee[J]. Science of the Total Environment, 2022, 842: 156819.
    [72] ZHU LY, WANG KW, WU XM, ZHENG H, LIAO XJ. Association of specific gut microbiota with polyethylene microplastics caused gut dysbiosis and increased susceptibility to opportunistic pathogens in honeybees[J]. Science of the Total Environment, 2024, 918: 170642.
    [73] LI ZY, GUO DZ, WANG C, CHI XP, LIU ZG, WANG Y, WANG HF, GUO XQ, WANG NX, XU BH, GAO Z. Toxic effects of the heavy metal Cd on Apis cerana cerana (Hymenoptera: Apidae): oxidative stress, immune disorders and disturbance of gut microbiota[J]. Science of the Total Environment, 2024, 912: 169318.
    [74] ENGEL P, KWONG WK, McFREDERICK Q, ANDERSON KE, BARRIBEAU SM, CHANDLER JA, SCOTT CORNMAN R, DAINAT J, de MIRANDA JR, DOUBLET V, EMERY O, EVANS JD, FARINELLI L, FLENNIKEN ML, GRANBERG F, GRASIS JA, GAUTHIER L, HAYER J, KOCH H, KOCHER S, et al. The bee microbiome: impact on bee health and model for evolution and ecology of host-microbe interactions[J]. mBio, 2016, 7(2): e02164-15.
    [75] STEELE MI, MOTTA EVS, GATTU T, MARTINEZ D, MORAN NA. The gut microbiota protects bees from invasion by a bacterial pathogen[J]. Microbiology Spectrum, 2021, 9(2): e0039421.
    [76] WU YQ, ZHENG YF, CHEN YN, WANG S, CHEN YP, HU FL, ZHENG HQ. Honey bee (Apis mellifera) gut microbiota promotes host endogenous detoxification capability via regulation of P450 gene expression in the digestive tract[J]. Microbial Biotechnology, 2020, 13(4): 1201-1212.
    [77] BONILLA-ROSSO G, ENGEL P. Functional roles and metabolic niches in the honey bee gut microbiota[J]. Current Opinion in Microbiology, 2018, 43: 69-76.
    [78] RAYMANN K, MORAN NA. The role of the gut microbiome in health and disease of adult honey bee workers[J]. Current Opinion in Insect Science, 2018, 26: 97-104.
    [79] KWONG WK, MANCENIDO AL, MORAN NA. Immune system stimulation by the native gut microbiota of honey bees[J]. Royal Society Open Science, 2017, 4(2): 170003.
    [80] MILLER DL, SMITH EA, NEWTON ILG. A bacterial symbiont protects honey bees from fungal disease[J]. mBio, 2021, 12(3): e0050321.
    [81] HUANG Q, LARIVIERE PJ, ELIJAH POWELL J, MORAN NA. Engineered gut symbiont inhibits microsporidian parasite and improves honey bee survival[J]. Proceedings of the National Academy of Sciences of the United States of America, 2023, 120(25): e2220922120.
    [82] DOSCH C, MANIGK A, STREICHER T, TEHEL A, PAXTON RJ, TRAGUST S. The gut microbiota can provide viral tolerance in the honey bee[J]. Microorganisms, 2021, 9(4): 871.
    [83] LANG HY, DUAN HJ, WANG JN, ZHANG WH, GUO J, ZHANG X, HU XS, ZHENG H. Specific strains of honeybee gut Lactobacillus stimulate host immune system to protect against pathogenic Hafnia alvei[J]. Microbiology Spectrum, 2022, 10(1): e0189621.
    [84] WU YQ, ZHENG YF, CHEN YN, CHEN GW, ZHENG HQ, HU FL. Apis cerana gut microbiota contribute to host health though stimulating host immune system and strengthening host resistance to Nosema ceranae[J]. Royal Society Open Science, 2020, 7(5): 192100.
    [85] ZENDO T, OHASHI C, MAENO S, PIAO XG, SALMINEN S, SONOMOTO K, ENDO A. Kunkecin A, a new nisin variant bacteriocin produced by the fructophilic lactic acid bacterium, Apilactobacillus kunkeei FF30-6 isolated from honey bees[J]. Frontiers in Microbiology, 2020, 11: 571903.
    [86] KOCH H, SCHMID-HEMPEL P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite[J]. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(48): 19288-19292.
    [87] KOCH H, SCHMID-HEMPEL P. Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host-parasite system[J]. Ecology Letters, 2012, 15(10): 1095-1103.
    [88] PALMER-YOUNG EC, RAFFEL TR, McFREDERICK QS. pH-mediated inhibition of a bumble bee parasite by an intestinal symbiont[J]. Parasitology, 2019, 146(3): 380-388.
    [89] PALMER-YOUNG EC, MARKOWITZ LM, HUANG WF, EVANS JD. High temperatures augment inhibition of parasites by a honey bee gut symbiont[J]. Applied and Environmental Microbiology, 2023, 89(10): e0102323.
    [90] LI JH, EVANS JD, LI WF, ZHAO YZ, DEGRANDI-HOFFMAN G, HUANG SK, LI ZG, HAMILTON M, CHEN YP. New evidence showing that the destruction of gut bacteria by antibiotic treatment could increase the honey bee’s vulnerability to Nosema infection[J]. PLoS One, 2017, 12(11): e0187505.
    [91] LANG HY, WANG H, WANG HQ, ZHONG ZP, XIE XB, ZHANG WH, GUO J, MENG L, HU XS, ZHANG X, ZHENG H. Engineered symbiotic bacteria interfering Nosema redox system inhibit microsporidia parasitism in honeybees[J]. Nature Communications, 2023, 14(1): 2778.
    [92] ZHENG H, ELIJAH POWELL J, STEELE MI, DIETRICH C, MORAN NA. Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling[J]. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114(18): 4775-4780.
    [93] KE?NEROVá L, MARS RAT, ELLEGAARD KM, TROILO M, SAUER U, ENGEL P. Disentangling metabolic functions of bacteria in the honey bee gut[J]. PLoS Biology, 2017, 15(12): e2003467.
    [94] ZHANG ZJ, MU XH, SHI Y, ZHENG H. Distinct roles of honeybee gut bacteria on host metabolism and neurological processes[J]. Microbiology Spectrum, 2022, 10(2): e0243821.
    [95] LIBERTI J, KAY T, QUINN A, KESNER L, FRANK ET, CABIROL A, RICHARDSON TO, ENGEL P, KELLER L. The gut microbiota affects the social network of honeybees[J]. Nature Ecology & Evolution, 2022, 6(10): 1471-1479.
    [96] WANG XF, ZHONG ZP, CHEN XY, HONG ZY, LIN WM, MU XH, HU XS, ZHENG H. High-fat diets with differential fatty acids induce obesity and perturb gut microbiota in honey bee[J]. International Journal of Molecular Sciences, 2021, 22(2): 834.
    [97] MOTTA EVS, ELIJAH POWELL J, LEONARD SP, MORAN NA. Prospects for probiotics in social bees[J]. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 2022, 377(1853): 20210156.
    [98] LIU BQ, BAO XY, YAN JY, ZHANG D, SUN X, LI CQ, CHEN ZB, LUAN JB. Rickettsia symbionts spread via mixed mode transmission, increasing female fecundity and sex ratio shift by host hormone modulating[J]. Proceedings of the National Academy of Sciences of the United States of America, 2024, 121(25): e2406788121.
    [99] ROBINSON GE, PAGE REJr, STRAMBI C, STRAMBI A. Hormonal and genetic control of behavioral integration in honey bee colonies[J]. Science, 1989, 246(4926): 109-112.
    [100] SULLIVAN JP, JASSIM O, FAHRBACH SE, ROBINSON GE. Juvenile hormone paces behavioral development in the adult worker honey bee[J]. Hormones and Behavior, 2000, 37(1): 1-14.
    [101] AMENT SA, WANG Y, ROBINSON GE. Nutritional regulation of division of labor in honey bees: toward a systems biology perspective[J]. Wiley Interdisciplinary Reviews Systems Biology and Medicine, 2010, 2(5): 566-576.
    [102] BAJGAR A, JINDRA M, DOLEZEL D. Autonomous regulation of the insect gut by circadian genes acting downstream of juvenile hormone signaling[J]. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(11): 4416-4421.
    [103] WU JH, WANG QQ, WANG DD, WONG ACN, WANG GH. Axenic and gnotobiotic insect technologies in research on host-microbiota interactions[J]. Trends in Microbiology, 2023, 31(8): 858-871.
    [104] MARU??áKOVá IC, SCHUSTEROVá P, BIELIK B, TOPOR?áK J, BíLIKOVá K, MUDRO?OVá D. Effect of application of probiotic pollen suspension on immune response and gut microbiota of honey bees (Apis mellifera)[J]. Probiotics and Antimicrobial Proteins, 2020, 12(3): 929-936.
    [105] ELLEGAARD KM, BROCHET S, BONILLA-ROSSO G, EMERY O, GLOVER N, HADADI N, JARON KS, van der MEER JR, ROBINSON-RECHAVI M, SENTCHILO V, TAGINI F, SAGE CLASS 2016-17, ENGEL P. Genomic changes underlying host specialization in the bee gut symbiont Lactobacillus Firm5[J]. Molecular Ecology, 2019, 28(9): 2224-2237.
    [106] ENGEL P, MARTINSON VG, MORAN NA. Functional diversity within the simple gut microbiota of the honey bee[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(27): 11002-11007.
    [107] ZHENG H, NISHIDA A, KWONG WK, KOCH H, ENGEL P, STEELE MI, MORAN NA. Metabolism of toxic sugars by strains of the bee gut symbiont Gilliamella apicola[J]. mBio, 2016, 7(6): e01326-16.
    [108] LEE FJ, MILLER KI, McKINLAY JB, NEWTON ILG. Differential carbohydrate utilization and organic acid production by honey bee symbionts[J]. FEMS Microbiology Ecology, 2018, 94(8). DOI: 10.1101/294249.
    [109] LI YY, LEONARD SP, ELIJAH POWELL J, MORAN NA. Species divergence in gut-restricted bacteria of social bees[J]. Proceedings of the National Academy of Sciences of the United States of America, 2022, 119(18): e2115013119.
    [110] WANG JN, LANG HY, ZHANG WH, ZHAI YF, ZHENG L, CHEN H, LIU Y, ZHENG H. Stably transmitted defined microbial community in honeybees preserves Hafnia alvei inhibition by regulating the immune system[J]. Frontiers in Microbiology, 2022, 13: 1074153.
    [111] ELIJAH POWELL J, CARVER Z, LEONARD SP, MORAN NA. Field-realistic tylosin exposure impacts honey bee microbiota and pathogen susceptibility, which is ameliorated by native gut probiotics[J]. Microbiology Spectrum, 2021, 9(1): e0010321.
    [112] DAISLEY BA, PITEK AP, CHMIEL JA, AL KF, CHERNYSHOVA AM, FARAGALLA KM, BURTON JP, THOMPSON GJ, REID G. Novel probiotic approach to counter Paenibacillus larvae infection in honey bees[J]. The ISME Journal, 2020, 14: 476-491.
    [113] STEPHAN JG, LAMEI S, PETTIS JS, RIESBECK K, de MIRANDA JR, FORSGREN E. Honeybee-specific lactic acid bacterium supplements have no effect on American foulbrood-infected honeybee colonies[J]. Applied and Environmental Microbiology, 2019, 85(13): e00606-19.
    [114] LAMEI S, STEPHAN JG, NILSON B, SIEUWERTS S, RIESBECK K, de MIRANDA JR, FORSGREN E. Feeding honeybee colonies with honeybee-specific lactic acid bacteria (hbs-LAB) does not affect colony-level hbs-LAB composition or Paenibacillus larvae spore levels, although American foulbrood affected colonies harbor a more diverse hbs-LAB community[J]. Microbial Ecology, 2020, 79(3): 743-755.
    [115] DAISLEY BA, PITEK AP, TORRES C, LOWERY R, ADAIR BA, AL KF, NI?O B, BURTON JP, ALLEN-VERCOE E, THOMPSON GJ, REID G, NI?O E. Delivery mechanism can enhance probiotic activity against honey bee pathogens[J]. The ISME Journal, 2023, 17(9): 1382-1395.
    [116] LEONARD SP, ELIJAH POWELL J, PERUTKA J, GENG P, HECKMANN LC, HORAK RD, DAVIES BW, ELLINGTON AD, BARRICK JE, MORAN NA. Engineered symbionts activate honey bee immunity and limit pathogens[J]. Science, 2020, 367(6477): 573-576.
    [117] ENGEL P, MORAN NA. The gut microbiota of insects: diversity in structure and function[J]. FEMS Microbiology Reviews, 2013, 37(5): 699-735.
    [118] LEONARD SP, PERUTKA J, ELIJAH POWELL J, GENG P, RICHHART DD, BYROM M, KAR S, DAVIES BW, ELLINGTON AD, MORAN NA, BARRICK JE. Genetic engineering of bee gut microbiome bacteria with a toolkit for modular assembly of broad-host-range plasmids[J]. ACS Synthetic Biology, 2018, 7(5): 1279-1290.
    [119] LARIVIERE PJ, LEONARD SP, HORAK RD, ELIJAH POWELL J, BARRICK JE. Honey bee functional genomics using symbiont-mediated RNAi[J]. Nature Protocols, 2023, 18(3): 902-928.
    [120] KIKUCHI Y, HAYATSU M, HOSOKAWA T, NAGAYAMA A, TAGO K, FUKATSU T. Symbiont-mediated insecticide resistance[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(22): 8618-8622.
    [121] KIKUCHI Y, HOSOKAWA T, FUKATSU T. An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts[J]. The ISME Journal, 2011, 5(3): 446-460.
    [122] MENG YJ, LI S, ZHANG C, ZHENG H. Strain-level profiling with picodroplet microfluidic cultivation reveals host-specific adaption of honeybee gut symbionts[J]. Microbiome, 2022, 10(1): 140.
    [123] ZHANG B, LEONARD SP, LI YY, MORAN NA. Obligate bacterial endosymbionts limit thermal tolerance of insect host species[J]. Proceedings of the National Academy of Sciences of the United States of America, 2019, 116(49): 24712-24718.
    [124] CHENG XW, WANG C, YANG JZ, LIU D, LIAO YT, WANG B, HAN SY, ZHANG X, ZHENG H, LU Y. Nanotransducer-enabled wireless spatiotemporal tuning of engineered bacteria in bumblebee[J]. Small, 2023, 19(36): e2301064.
    [125] LI LY, PAN HZ, PANG GJ, LANG HY, SHEN Y, SUN T, ZHANG YY, LIU J, CHANG J, KANG J, ZHENG H, WANG HJ. Precise thermal regulation of engineered bacteria secretion for breast cancer treatment in vivo[J]. ACS Synthetic Biology, 2022, 11(3): 1167-1177.
    [126] DIAZ T, DEL-VAL E, AYALA R, LARSEN J. Alterations in honey bee gut microorganisms caused by Nosema spp. and pest control methods[J]. Pest Management Science, 2019, 75(3): 835-843.
    [127] LI B, CAI XL, LI MY, WANG FX, ZOU CS, ZHANG JS, XIE MY, QI FH, JING TZ. Countering beta-cypermethrin: partitioning roles of the insect gut and its bacteria[J]. Journal of Pest Science, 2023, 96: 1243-1255.
    [128] DONG ZX, TANG QH, LI WL, WANG ZW, LI XJ, FU CM, LI D, QIAN K, TIAN WL, GU J. Honeybee (Apis mellifera) resistance to deltamethrin exposure by Modulating the gut microbiota and improving immunity[J]. Environmental pollution (Barking, Essex: 1987),2022, 314, 120340.
    [129] UGOLINI L, CILIA G, PAGNOTTA E, MALAGUTI L, CAPANO V, GUERRA I, ZAVATTA L, ALBERTAZZI S, MATTEO R, LAZZERI L, RIGHETTI L, NANETTI A. Glucosinolate bioactivation by Apis mellifera workers and its impact on Nosema ceranae infection at the colony level[J]. Biomolecules, 2021, 11(11): 1657.
    [130] YUAN XY, SUN JY, KADOWAKI T. Aspartyl protease in the secretome of honey bee trypanosomatid parasite contributes to infection of bees[J]. Parasites & Vectors, 2024, 17(1): 60.
    [131] MOTTA EVS, MAK M, de JONG TK, POWELL JE, O’DONNELL A, SUHR KJ, RIDDINGTON IM, MORAN NA. Oral or topical exposure to glyphosate in herbicide formulation impacts the gut microbiota and survival rates of honey bees[J]. Applied and Environmental Microbiology, 2020, 86(18): e01150-20.
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LIU Jianhui, CHEN Jing, HU Yueyang, WU Xiaobo. Research progress in temporospatial characteristics and functions of gut microbiota in honeybees. [J]. Acta Microbiologica Sinica, 2025, 65(3): 898-915

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  • Received:September 23,2024
  • Online: March 10,2025
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