The Relationship Between Gut Microflora and Sociality of Honeybee

doi:10.13560/j.cnki.biotech.bull.1985.2019-0876

Abstract

Abstract: Honeybees are the typical eusocial insects living in social groups. Compared with solitary insects,they harbor special gut microflora. The relationship between bees’ unique gut microbes and their sociability is a fascinating scientific issue. Guts of honey bee workers are dominated by 9 distinctive bacterial phylotypes. The dominant species and abundances vary among various niche of digestive tract. There are few bacterial phylotypes and low abundance in foregut,but rich phylotypes and high abundances in hindgut,accounting for over 99% of microbes in whole gut. The microflora varies among the bees with different social division. Honeybee gut microbes can regulate their castes differentiation,social labor division,food intake behavior and lifespan by affecting insulin signals,the synthesis of juvenile hormone and vitellogenin,and the antioxidant stress ability. Besides,gut microbes in honeybee also play roles in activating immunity,inhibiting pathogenic bacteria,degrading food,promoting nutrient absorption,detoxifying,and fermenting honey and bee bread. The profile of honeybee gut microbes and the relationship between gut microbes and honeybee sociality are reviewed in this paper.

Key words: honeybee, gut, microflora, castes differentiation, social division, lifespan

WANG Hong-fang, XU Bao-hua. The Relationship Between Gut Microflora and Sociality of Honeybee[J]. Biotechnology Bulletin, 2020, 36(2): 71-76.

References

[1] White PB.The normal bacterial flora of the honey bee[J]. J Pathol Bacteriol, 1921, 24:64-78.
[2] Lotmar R.Uber flagellaten und akterien in Diinndarm der Honigbiene(Apis vicllifica)[J]. Schweiz Bienen-Ztg, 1946, 2:49-76.
[3] Gilliam M.Microbial sterility of the intestinal content of the immature honey bee, Apis mellifera[J]. Ann Entomol Soc Am, 1971, 64:315-316.
[4] Kluge R.Untersuchungen über die Darmflora der Honigbiene, Apis mellifera[J]. Z Bienenforsch, 1963, 6:141-69.
[5] Gilliam M, Prest DB.Microbiology of feces of the larval honey bee, Apis mellifera[J]. J Invertebr Pathol, 1987, 49:70-75.
[6] Zheng H, Steele MI, Leonard SP, et al.Honey bees as models for gut microbiota research. Lab Anim(NY), 2018, 47(11):317-325.
[7] Jeyaprakash A, Hoy MA, Allsopp MH.Bacterial diversity in worker adults of Apis mellifera capensis and Apis mellifera scutellata(Insecta:Hymenoptera)assessed using 16S rRNA sequences[J]. J Invertebr Pathol, 2003, 84:96-103.
[8] Babendreier D, Joller D, Romeis J, et al.Bacterial community structures in honeybee intestines and their response to two insecti-cidal proteins[J]. FEMS Microbiol Ecol, 2007, 59:600-610.
[9] Moran NA, Hansen AK, Powell JE, et al.Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees[J]. PLoS One, 2012, 7:e36393.
[10] Sabree ZL, Hansen AK, Moran NA.Independent studies using deep sequencing resolve the same set of core bacterial species dominating gut communities of honey bees[J]. PLoS One, 2012, 7:e41250.
[11] Kwong WK, Moran NA.Cultivation and characterization of the gut symbionts of honey bees and bumble bees:description of Snodgrassella alvi gen. nov. , sp. nov. , a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov. , sp. nov. , a member of Orbaceae fam. nov. , Orbales ord. nov. , a sister taxon to the order ‘Enterobacteriales’ of the Gammaproteobacteria[J]. Int J Syst Evol Microbiol, 2013, 63:2008-2018.
[12] Martinson VG, Danforth BN, Minckley RL, et al.A simple and distinctive microbiota associated with honey bees and bumble bees[J]. Mol Ecol, 2011, 20:619-628.
[13] Martinson VG, Moy J, Moran NA.Establishment of characteristic gut bacteria during development of the honeybee worker[J]. Appl Environ Microbiol, 2012, 78:2830-2840.
[14] Powell JE, Martinson VG, Urban-Mead K, et al.Routes of acquisition of the gut microbiota of Apis mellifera[J]. Appl Environ Microbiol, 2014, 80:7378-7387.
[15] Scardovi V, Trovatelli D.New species of Bifidobacteria from Apis mellifica L and Apis indica F. A contribution to the taxonomy and biochemistry of the genus Bifidobacterium[J]. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg, 1969, 123:64-88.
[16] Bottacini F, et al.Bifidobacterium asteroides PRL2011 genome analysis reveals clues for colonization of the insect gut[J]. PLoS One, 2012, 7:e44229.
[17] Engel P, Kwong WK, Moran NA.Frischella perrara gen. nov. , sp. nov. , a gammaproteobacterium isolated from the gut of the honeybee, Apis mellifera[J]. Int J Syst Evol Microbiol, 2013, 63:3646-3651.
[18] Corby-Harris V, Maes P, Anderson KE.The bacterial communities associated with honey bee(Apis mellifera)foragers[J]. PLoS One, 2014, 9:e95056.
[19] Kešnerová L, Moritz R, Engel P.Bartonella apis sp. nov. , a honey bee gut symbiont of the class Alphaproteobacteria[J]. Int J Syst Evol Microbiol, 2016, 66(1):414-421.
[20] Engel P, Bartlett KD, Moran NA.The bacterium Frischella perrara causes scab formation in the gutof its honeybee host[J]. MBio, 2015, 6:e00193-15.
[21] Corby-Harris V, Snyder LA, Schwan MR, et al.Origin and effect of Alpha 2. 2 Acetobacteraceae in honey bee larvae and description of Parasaccharibacter apium gen. nov. , sp. nov[J]. Appl Environ Microbiol, 2014, 80:7460-7472.
[22] Anderson KE, Sheehan TH, Mott BM, et al.Microbial ecology of the hive and pollination landscape:bacterial associates from floral nectar, the alimentary tract and stored food of honey bees(Apis mellifera)[J]. PLoS One, 2013, 8:e83125.
[23] Anderson KE, Carroll MJ, Sheehan T, et al.Hive-stored pollen of honey bees:many lines of evidence are consistent with pollen preservation, not nutrient conversion[J]. Mol Ecol, 2014, 23:5904-5917.
[24] Corby-Harris V, Maes P, Anderson KE.The bacterial communities associated with Honey Bee(Apis mellifera)foragers[J]. PLoS One, 2014, 9(4):e95056.
[25] Olofsson TC, Vasquez A.Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera[J]. Current Microbiology, 2008, 57:356-363.
[26] Va’squez A, Olofsson TC, Sammataro D.A scientific note on the lactic acid bacterial flora in honeybees in the USA - A comparison with bees from Sweden[J]. Apidologie, 2009, 40:26-28.
[27] Olofsson TC, Va’squez A, Sammataro D, et al.A scientific note on the lactic acid bacterial flora within the honeybee subspecies;Apis mellifera(Buckfast), A. m. scutellata, A. m. mellifera, and A. m. monticola[J]. Apidologie, 2011, 42(6):696-699.
[28] Ludvigsen J, Rangberg A, Avershina E, et al.Shifts in the midgut/pyloric microbiota composition within a honey bee apiary throughout a season[J]. Microbes Environ, 2015, 30(3):235-244.
[29] Kwong WK, Moran NA.Gut microbial communities of social bees[J]. Nat Rev Microbiol, 2016, 14(6):374-384.
[30] Kapheim KM, Rao VD, Yeoman CJ, et al.Caste-specific differences in hindgut microbial communities of honey bees(Apis mellifera)[J]. PLoS One, 2015, 10(4):e0123911.
[31] Powell JE, Eiri D, Moran NA, et al.Modulation of the honey bee queen microbiota:Effects of early social contact[J]. PLoS One, 2018, 13(7):e0200527.
[32] Anderson KE, Ricigliano VA, Mott BM, et al.The queen’s gut refines with age:longevity phenotypes in a social insect model[J]. Microbiome, 2018, 6:108.
[33] Wolschin F, Mutti NS, Amdam GV.Insulin receptor substrate influences female caste development in honeybees[J]. Biol Lett, 2011, 7(1):112-115.
[34] Shin SC, Kim SH, You H, et al.Drosophila microbiome modulates host developmental and metabolic homeostasis via insulinsignaling[J]. Science, 2011, 334(6056):670-674.
[35] Zheng H, Powell JE, Steele MI, et al.Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling[J]. Proc Natl Acad Sci USA, 2017, 114:4775-4780.
[36] Kešnerová L, Mars RAT, Ellegaard KM, et al.Disentangling metabolic functions of bacteria in the honey bee gut[J]. PLoS Biol, 2017, 15:e2003467.
[37] Rachinsky A, Strambi C, Strambi A, et al.Caste and metamorphosis:hemolymph titers of juvenile hormone and ecdysteroids in last instar honeybee larvae[J]. Gen Comp Endocrinol, 1990, 79(1):31-38.
[38] Rembold H.Caste specific modulation of juvenile-hormone titers in Apis mellifera[J]. Insect Biochem, 1987, 17(7):1003-1006.
[39] Schwarz RS, Moran NA, Evans JD.Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers[J]. Proc Natl Acad Sci USA, 2016, 113(33):9345-9350.
[40] Amdam GV, Omholt SW.The hive bee to forager transition in honeybee colonies:The double repressor hypothesis[J]. J Theor Biol, 2003, 223:451-464.
[41] Guidugli KR, Nascimento AM, Amdam GV, et al.Vitellogenin regulates hormonal dynamics in the worker caste of a eusocial insect[J]. FEBS Lett, 2005, 579:4961-4965.
[42] Nelson CM, Ihle KE, Fondrk MK, et al.The Gene vitellogenin has multiple coordinating effects on social organization[J]. PLoS Biol, 2007, 5(3):e62.
[43] Harris JW, Woodring J.Effects of stress, age, season, and source colony on levels of octopamine, dopamine and serotonin in the honey bee(Apis mellifera L.)brain[J]. J Insect Physiol, 1992, 38, 29-35.
[44] Jones JC, Fruciano C, Marchant J, et al.The gut microbiome is associated with behavioural task in honey bees[J]. Insectes Soc, 2018, 65(3):419-429.
[45] Amdam GV, Omholt SW.The regulatory anatomy of honeybee lifespan[J]. J Theor Biol, 2002, 216:209-28.
[46] Amdam GV, Simões ZLP, Hagen A, et al.Hormonal control of the yolk precursor vitellogenin regulates immune function and longevity in honeybees[J]. Exp Gerontol, 2004, 39:767-73.
[47] Seehuus SC, Norberg K, Gimsa U, et al.Reproductive protein protects functionally sterile honey bee workers from oxidative stress[J]. Proc Natl Acad Sci, 2006, 103:962-7.
[48] Corona M, Velarde RA, Remolina S, et al.Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity[J]. Proc Natl Acad Sci, 2007, 104:7128-33.
[49] Maes PW, Rodrigues PAP, Oliver R, et al.Diet-related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honeybee(Apis mellifera)[J]. Mol Ecol, 2016, 25:5439-5450.
[50] Schwarz RS, Huang Q, Evans JD.Hologenome theory and the honey bee pathosphere[J]. Curr Opin Insect Sci, 2015, 10:1-7.
[51] Koch H, Schmid-Hempel P.Socially transmitted gut microbiota protect bumble bees against an intestinal parasite[J]. Proc Natl Acad Sci USA, 2011, 108:19288-19292.
[52] Cariveau DP, Powell JE, Koch H, et al.Variation in gut microbial communities and its association with pathogen infection in wild bumble bees(Bombus)[J]. ISME J, 2014, 12:2369-2379.
[53] Koch H, Schmid-Hempel P.Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host-parasite system[J]. Ecol Lett, 2012, 15:1095-1103.
[54] Forsgren E, Olofsson TC, Vásquez A, et al.Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae[J]. Apidologie, 2010, 41:99-108.
[55] Wu M, Sugimura Y, Takaya N, et al.Characterization of bifidobacteria in the digestive tract of the Japanese honeybee, Apis cerana japonica[J]. J Invertebr Pathol, 2013, 112:88-93.
[56] Engel P, Martinson VG, Moran NA.Functional diversity within the simple gut microbiota of the honey bee[J]. Proc Natl Acad Sci USA, 2012, 109:11002-11007.
[57] Ellegaard KM, Tamarit D, Javelind E, et al.Extensive intra-phylotype diversity in Lactobacilli and Bifidobacteria from the honeybee gut[J]. BMC Genomics, 2015, 16:284.
[58] Kwong WK, Mancenido AL, Moran NA.Genome sequences of Lactobacillus sp. strains wkB8 and wkB10, members of the Firm-5 clade, from honey bee guts[J]. Genome Announc, 2014, 13:e01176-14.