Abstract
The recent worldwide decline of honey bee colonies is a major ecological problem which also threatens pollinated crop production. Several interacting stressors such as environmental pressures and pathogens are suspected. Recently, the gut microbiota has emerged as a critical factor affecting bee health and fitness. We profiled the bacterial communities associated with the gut and whole body of worker bees to assess whether non-thriving colonies could be separated from thriving hives based on their microbial signature. The microbiota of thriving colonies was characterised by higher diversity and higher relative abundance of bacterial taxa involved in sugar degradation that were previously associated with healthy bees (e.g. Commensalibacter sp. and Bartonella apis). In contrast, the microbiota of non-thriving bees was depleted in health-associated species (e.g. Lactobacillus apis), and bacterial taxa associated with disease states (e.g. Gilliamella apicola) and pollen degradation (e.g. G. apicola and Bifidobacterium asteroides) were present in higher abundance compared to thriving colonies. Gut and whole-body microbiota shared a similar dominant core but their comparison showed differences in composition and relative abundance. More differences in taxon relative abundance between gut and whole body were observed in non-thriving bees, suggesting that microbiota associated with other bee organs might also be different. Thus, microbiota profiling could be used as a diagnostic tool in beekeeping practices to predict hive health and guide hive management.
Similar content being viewed by others
References
Klein A-M, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci. 274:303–313. https://doi.org/10.1098/rspb.2006.3721
Gallai N, Salles JM, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68:810–821. https://doi.org/10.1016/j.ecolecon.2008.06.014
vanEngelsdorp D, Meixner MD (2010) A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J. Invertebr. Pathol. 103:S80–S95. https://doi.org/10.1016/j.jip.2009.06.011
Rucker RR, Thurman WN, Burgett M (2012) Honey bee pollination markets and the internalization of reciprocal benefits. Am. J. Agric. Econ. 94:956–977. https://doi.org/10.1093/ajae/aas031
Dukas R (2008) Mortality rates of honey bees in the wild. Insect. Soc. 55:252–255. https://doi.org/10.1007/s00040-008-0995-4
Neumann P, Carreck NL (2010) Honey bee colony losses. J. Apic. Res. 49:1–6. https://doi.org/10.3896/IBRA.1.49.1.01
vanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, Nguyen BK, Frazier M, Frazier J, Cox-Foster D, Chen Y, Underwood R, Tarpy DR, Pettis JS (2009) Colony collapse disorder: a descriptive study. PLoS One 4:e6481. https://doi.org/10.1371/journal.pone.0006481
McMenamin AJ, Genersch E (2015) Honey bee colony losses and associated viruses. Curr Opin Insect Sci 8:121–129. https://doi.org/10.1016/j.cois.2015.01.015
Goulson D, Nicholls E, Botias C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science (80- ) 347:1255957–1255957 .https://doi.org/10.1126/science.1255957
Barron AB (2015) Death of the bee hive: understanding the failure of an insect society. Curr Opin Insect Sci 10:45–50. https://doi.org/10.1016/j.cois.2015.04.004
Nazzi F, Pennacchio F (2014) Disentangling multiple interactions in the hive ecosystem. Trends Parasitol. 30:556–561. https://doi.org/10.1016/j.pt.2014.09.006
Evans JD, Schwarz RS (2011) Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol. 19:614–620. https://doi.org/10.1016/j.tim.2011.09.003
Genersch E (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl. Microbiol. Biotechnol. 87:87–97. https://doi.org/10.1007/s00253-010-2573-8
Crotti E, Sansonno L, Prosdocimi EM, Vacchini V, Hamdi C, Cherif A, Gonella E, Marzorati M, Balloi A (2013) Microbial symbionts of honeybees: a promising tool to improve honeybee health. New Biotechnol. 30:716–722. https://doi.org/10.1016/j.nbt.2013.05.004
Engel P, Kwong WK, McFrederick Q et al (2016) The bee microbiome: impact on bee health and model for evolution and ecology of host-microbe interactions. MBio 7:1–9. https://doi.org/10.1128/mBio.02164-15.Invited
de Vos WM, de Vos EA (2012) Role of the intestinal microbiome in health and disease: from correlation to causation. Nutr. Rev. 70:S45–S56. https://doi.org/10.1111/j.1753-4887.2012.00505.x
Anderson KE, Ricigliano VA (2017) Honey bee gut dysbiosis: a novel context of disease ecology. Curr Opin Insect Sci 22:125–132. https://doi.org/10.1016/j.cois.2017.05.020
Jeyaprakash A, Hoy MA, Allsopp MH (2003) Bacterial diversity in worker adults of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) assessed using 16S rRNA sequences. J. Invertebr. Pathol. 84:96–103. https://doi.org/10.1016/j.jip.2003.08.007
Kwong WK, Medina LA, Koch H, Sing KW, Soh EJY, Ascher JS, Jaffé R, Moran NA (2017) Dynamic microbiome evolution in social bees. Sci. Adv. 3:1–16. https://doi.org/10.1126/sciadv.1600513
Leonhardt SD, Kaltenpoth M (2014) Microbial communities of three sympatric Australian stingless bee species. PLoS One 9:e105718. https://doi.org/10.1371/journal.pone.0105718
Martinson VG, Danforth BN, Minckley RL et al (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Mol. Ecol. 20:619–628. https://doi.org/10.1111/j.1365-294X.2010.04959.x
Martinson VG, Moy J, Moran NA (2012) Establishment of characteristic gut bacteria during development of the honeybee worker. Appl. Environ. Microbiol. 78:2830–2840. https://doi.org/10.1128/AEM.07810-11
Powell JE, Martinson VG, Urban-Mead K, Moran NA (2014) Routes of acquisition of the gut microbiota of the honey bee Apis mellifera. Appl. Environ. Microbiol. 80:7378–7387. https://doi.org/10.1128/AEM.01861-14
Sabree ZL, Hansen AK, Moran NA (2012) Independent studies using deep sequencing resolve the same set of core bacterial species dominating gut communities of honey bees. PLoS One 7:e41250. https://doi.org/10.1371/journal.pone.0041250
Kwong WK, Moran NA (2016) Gut microbial communities of social bees. Nat Rev Microbiol 14:374–384. https://doi.org/10.1038/nrmicro.2016.43
Anderson KE, Sheehan TH, Mott BM, Maes P, Snyder L, Schwan MR, Walton A, Jones BM, Corby-Harris V (2013) 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 8:e83125. https://doi.org/10.1371/journal.pone.0083125
Engel P, Martinson VG, Moran N a (2012) Functional diversity within the simple gut microbiota of the honey bee. Proc. Natl. Acad. Sci. 109:11002–11007. https://doi.org/10.1073/pnas.1202970109
Babendreier D, Joller D, Romeis J et al (2007) Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol. Ecol. 59:600–610. https://doi.org/10.1111/j.1574-6941.2006.00249.x
Kakumanu ML, Reeves AM, Anderson TD, Rodrigues RR, Williams MA (2016) Honey bee gut microbiome is altered by in-hive pesticide exposures. Front. Microbiol. 7:1–11. https://doi.org/10.3389/fmicb.2016.01255
Raymann K, Shaffer Z, Moran NA (2017) Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees. PLoS Biol. 15:e2001861. https://doi.org/10.1371/journal.pbio.2001861
Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, Moran NA, Quan PL, Briese T, Hornig M, Geiser DM, Martinson V, vanEngelsdorp D, Kalkstein AL, Drysdale A, Hui J, Zhai J, Cui L, Hutchison SK, Simons JF, Egholm M, Pettis JS, Lipkin WI (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318:283–287. https://doi.org/10.1126/science.1146498
Erban T, Ledvinka O, Kamler M, Nesvorna M, Hortova B, Tyl J, Titera D, Markovic M, Hubert J (2017) Honeybee (Apis mellifera)-associated bacterial community affected by American foulbrood: detection of Paenibacillus larvae via microbiome analysis. Sci. Rep. 7:5084. https://doi.org/10.1038/s41598-017-05076-8
Maes PW, Rodrigues PAP, Oliver R, Mott BM, Anderson KE (2016) Diet-related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honeybee (Apis mellifera). Mol. Ecol. 25:5439–5450. https://doi.org/10.1111/mec.13862
Horton MA, Oliver R, Newton IL (2015) No apparent correlation between honey bee forager gut microbiota and honey production. PeerJ 3:e1329. https://doi.org/10.7717/peerj.1329
Yu Z, Morrison M (2004) Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques 36:808–812. https://doi.org/10.2144/3605A0808
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17:10. https://doi.org/10.14806/ej.17.1.200
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537–7541. https://doi.org/10.1128/AEM.01541-09
Allard G, Ryan FJ, Jeffery IB, Claesson MJ (2015) SPINGO: a rapid species-classifier for microbial amplicon sequences. BMC Bioinformatics 16:1–8. https://doi.org/10.1186/s12859-015-0747-1
Pedrós-Alió C (2012) The rare bacterial biosphere. Annu. Rev. Mar. Sci. 4:449–466. https://doi.org/10.1146/annurev-marine-120710-100948
Sun Z, Lu Y, Zhang H, Kumar D, Liu B, Gong Y, Zhu M, Zhu L, Liang Z, Kuang S, Chen F, Hu X, Cao G, Xue R, Gong C (2016) Effects of BmCPV infection on silkworm Bombyx mori intestinal bacteria. PLoS One 11:1–17. https://doi.org/10.1371/journal.pone.0146313
Wang W-W, He C, Cui J, Wang HD, Li ML (2014) Comparative analysis of the composition of intestinal bacterial communities in Dastarcus helophoroides fed different diets. J. Insect Sci. 14:1–13. https://doi.org/10.1673/031.014.111
Mockler BK, Kwong WK, Moran NA, Koch H (2018) Microbiome structure influences infection by the parasite Crithidia bombi in bumble bees. Appl Environ Microbiol AEM.02335–17 .https://doi.org/10.1128/AEM.02335-17
Kwong WK, Moran NA (2016) Apibacter adventoris gen. nov., sp. nov., a member of the phylum Bacteroidetes isolated from honey bees. Int. J. Syst. Evol. Microbiol. 66:1323–1329. https://doi.org/10.1099/ijsem.0.000882
Praet J, Aerts M, de Brandt E et al (2016) Apibacter mensalis sp. Nov.: a rare member of the bumblebee gut microbiota. Int. J. Syst. Evol. Microbiol. 66:1645–1651. https://doi.org/10.1099/ijsem.0.000921
Alberoni D, Baffoni L, Gaggìa F, Ryan PM, Murphy K, Ross PR, Stanton C, di Gioia D (2018) Impact of beneficial bacteria supplementation on the gut microbiota, colony development and productivity of Apis mellifera L. Benef Microbes 9:269–278. https://doi.org/10.3920/BM2017.0061
Hubert J, Bicianova M, Ledvinka O, Kamler M, Lester PJ, Nesvorna M, Kopecky J, Erban T (2017) Changes in the bacteriome of honey bees associated with the parasite Varroa destructor, and pathogens Nosema and Lotmaria passim. Microb. Ecol. 73:685–698. https://doi.org/10.1007/s00248-016-0869-7
Rothman JA, Carroll MJ, Meikle WG, Anderson KE, McFrederick QS (2018) Longitudinal effects of supplemental forage on the honey bee (Apis mellifera) microbiota and inter- and intra-colony variability. Microb. Ecol. 76:1–11. https://doi.org/10.1007/s00248-018-1151-y
Hamady M, Knight R (2009) Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res. 19:1141–1152. https://doi.org/10.1101/gr.085464.108
Moran NA, Hansen AK, Powell JE, Sabree ZL (2012) Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS One 7:1–10. https://doi.org/10.1371/journal.pone.0036393
Crailsheim K (1998) Trophallactic interactions in the adult honeybee (Apis mellifera L.). Apidologie 29:97–112. https://doi.org/10.1051/apido:19980106
Cariveau DP, Elijah Powell J, Koch H, Winfree R, Moran NA (2014) Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). ISME J 8:2369–2379. https://doi.org/10.1038/ismej.2014.68
Kapheim KM, Rao VD, Yeoman CJ, Wilson BA, White BA, Goldenfeld N, Robinson GE (2015) Caste-specific differences in hindgut microbial communities of honey bees (Apis mellifera). PLoS One 10:1–14. https://doi.org/10.1371/journal.pone.0123911
Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JBH, Matulich KL, Schmidt TM, Handelsman J (2012) Fundamentals of microbial community resistance and resilience. Front. Microbiol. 3:417. https://doi.org/10.3389/fmicb.2012.00417
Vásquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, Szekely L, Olofsson TC (2012) Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS One 7:e33188. https://doi.org/10.1371/journal.pone.0033188
Endo A, Salminen S (2013) Honeybees and beehives are rich sources for fructophilic lactic acid bacteria. Syst. Appl. Microbiol. 36:444–448. https://doi.org/10.1016/j.syapm.2013.06.002
Asama T, Arima TH, Gomi T, Keishi T, Tani H, Kimura Y, Tatefuji T, Hashimoto K (2015) Lactobacillus kunkeei YB38 from honeybee products enhances IgA production in healthy adults. J. Appl. Microbiol. 119:818–826. https://doi.org/10.1111/jam.12889
Kešnerová L, Mars RAT, Ellegaard KM, Troilo M, Sauer U, Engel P (2017) Disentangling metabolic functions of bacteria in the honey bee gut. PLoS Biol. 15:e2003467. https://doi.org/10.1371/journal.pbio.2003467
Ludvigsen J, Porcellato D, L’Abée-Lund TM et al (2017) Geographically widespread honeybee-gut symbiont subgroups show locally distinct antibiotic-resistant patterns. Mol. Ecol. 26:6590–6607. https://doi.org/10.1111/mec.14392
Ellegaard KM, Tamarit D, Javelind E, Olofsson TC, Andersson SGE, Vásquez A (2015) Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut. BMC Genomics 16:1–22. https://doi.org/10.1186/s12864-015-1476-6
Segers FH, Kešnerová L, Kosoy M, Engel P (2017) Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen. ISME J 11:1232–1244. https://doi.org/10.1038/ismej.2016.201
Crotti E, Rizzi A, Chouaia B, Ricci I, Favia G, Alma A, Sacchi L, Bourtzis K, Mandrioli M, Cherif A, Bandi C, Daffonchio D (2010) Acetic acid bacteria, newly emerging symbionts of insects. Appl. Environ. Microbiol. 76:6963–6970. https://doi.org/10.1128/AEM.01336-10
Schwarz RS, Moran NA, Evans JD (2016) Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers. Proc. Natl. Acad. Sci. 113:9345–9350. https://doi.org/10.1073/pnas.1606631113
Cornman RS, Tarpy DR, Chen Y, Jeffreys L, Lopez D, Pettis JS, vanEngelsdorp D, Evans JD (2012) Pathogen webs in collapsing honey bee colonies. PLoS One 7:e43562. https://doi.org/10.1371/journal.pone.0043562
Aizenberg-Gershtein Y, Izhaki I, Halpern M (2013) Do honeybees shape the bacterial community composition in floral nectar? PLoS One 8:e67556. https://doi.org/10.1371/journal.pone.0067556
McFrederick QS, Wcislo WT, Taylor DR et al (2012) Environment or kin: whence do bees obtain acidophilic bacteria? Mol. Ecol. 21:1754–1768. https://doi.org/10.1111/j.1365-294X.2012.05496.x
Corby-Harris V, Snyder LA, Schwan MR, Maes P, McFrederick QS, Anderson KE (2014) Origin and effect of alpha 2.2 Acetobacteraceae in honey bee larvae and description of Parasaccharibacter apium gen. nov., sp. nov. Appl. Environ. Microbiol. 80:7460–7472. https://doi.org/10.1128/AEM.02043-14
Bartlewicz J, Lievens B, Honnay O, Jacquemyn H (2016) Microbial diversity in the floral nectar of Linaria vulgaris along an urbanization gradient. BMC Ecol. 16:1–11. https://doi.org/10.1186/s12898-016-0072-1
Peix A, Ramírez-Bahena MH, Velázquez E (2009) Historical evolution and current status of the taxonomy of genus Pseudomonas. Infect. Genet. Evol. 9:1132–1147. https://doi.org/10.1016/j.meegid.2009.08.001
Sommer F, Anderson JM, Bharti R, Raes J, Rosenstiel P (2017) The resilience of the intestinal microbiota influences health and disease. Nat Rev Microbiol 15:630–638. https://doi.org/10.1038/nrmicro.2017.58
Kwong WK, Engel P, Koch H, Moran NA (2014) Genomics and host specialization of honey bee and bumble bee gut symbionts. Proc. Natl. Acad. Sci. 111:11509–11514. https://doi.org/10.1073/pnas.1405838111
Acknowledgments
We thank the beekeeper for allowing us to collect honey bee workers and for his assistance in conducting this survey. Work in PWOT’s lab was supported in part by Science Foundation Ireland through a Centre award to the APC Microbiome Ireland (SFI/12/RC/2273).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Ribière, C., Hegarty, C., Stephenson, H. et al. Gut and Whole-Body Microbiota of the Honey Bee Separate Thriving and Non-thriving Hives. Microb Ecol 78, 195–205 (2019). https://doi.org/10.1007/s00248-018-1287-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-018-1287-9