Shifts in the midgut/pyloric microbiota composition within a honey bee apiary throughout a season

Microbes and Environments

Volumn 30, Issue 3, 2015, Pages 235-244

  Ludvigsen, Jane ^a   Rangberg, Anbjørg ^a   Avershina, Ekaterina ^a   Sekelja, Monika ^a,b   Kreibich, Claus ^a   Amdam, Gro ^a,c   Rudi, Knut ^a  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b Genetic Analysis AS   (Norway)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Gilliamella apicola; Honey bee workers; Midgut pyloric microbiota; Seasonal changes; Snodgrassella alvi

Indexed keywords

ANIMAL; BACTERIUM; BEE; CLASSIFICATION; GASTROINTESTINAL TRACT; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTESTINE FLORA; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; SEASON;

ANIMALS; BACTERIA; BEES; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEASONS;

EID: 84942601969     PISSN: 13426311     EISSN: 13474405     Source Type: Journal    
DOI: 10.1264/jsme2.ME15019     Document Type: Article

References (56)

1. Amdam, G.V., K. Norberg, M.K. Fondrk, and R.E. Page 2004. Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees. Proc. Natl. Acad. Sci. U.S.A. 101:11350–11355
2. Anderson, K.E., T.H. Sheehan, B.M. Mott, P. Maes, L. Snyder, M.R. Schwan, A. Walton, B.M. Jones, and V. Corby-Harris. 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
3. Avershina, E., O. Storro, T. Oien, R. Johnsen, R. Wilson, T. Egeland, and K. Rudi. 2013. Bifidobacterial succession and correlation networks in a large unselected cohort of mothers and their children. Appl. Environ. Microbiol. 79:497–507
4. Brady, C., I. Cleenwerck, S. Venter, M. Vancanneyt, J. Swings, and T. Coutinho. 2008. Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst. Appl. Microbiol. 31: 447–460
5. Brady, C.L., S.N. Venter, I. Cleenwerck, K. Vandemeulebroecke, P. De Vos, and T.A. Coutinho. 2010. Transfer of Pantoea citrea, Pantoea punctata and Pantoea terrea to the genus Tatumella emend. as Tatumella citrea comb. nov., Tatumella punctata comb. nov. and Tatumella terrea comb. nov. and description of Tatumella morbirosei sp. nov. Int. J. Syst. Evol. Microbiol. 60:484–494
6. Caporaso, J.G., J. Kuczynski, J. Stombaugh, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336
7. Chandler, J.A., J.M. Lang, S. Bhatnagar, J.A. Eisen, and A. Kopp. 2011. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLoS Genet. 7:e1002272
8. Cooper, D.P., M.W. Schaffer, and L.S. Buchmann. 1985. Temperature regulationof honey bees (Apis mellifera) foraging in the sonoran desert. J. Exp. Biol.:1–15
9. Corby-Harris, V., P. Maes, and K.E. Anderson. 2014. The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS One 9:e95056
10. Crailsheim, K. 1988. Intestinal transport of sugars in the honeybee (Apis mellifera L.). J. Insect Physiol. 34:839–845
11. Crailsheim, K. 1990. The protein balance of the honey bee worker. Apidologie 21:417–429
12. David, L.A., C.F. Maurice, R.N. Carmody, et al. 2014. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505:559–563
13. Davis, F.C. 2004. Inside and outside influences, p. 145–157. In F.C. David (ed.), The Honey Bee Inside Out. Bee Craft Limited, Warwickshire.
14. De Filippo, C., D. Cavalieri, M. Di Paola, M. Ramazzotti, J.B. Poullet, S. Massart, S. Collini, G. Pieraccini, and P. Lionetti. 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. U.S.A. 107:14691–14696
15. DeSantis, T.Z. P Hugenholtz, N. Larsen, M. Rojas, E.L. Brodie, K. Keller, T. Huber, D. Dalevi, P. Hu, and G.L. Andersen. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72:5069–5072
16. Disayathanoowat, T., J.P. Young, T. Helgason, and P. Chantawannakul. 2012. T-RFLP analysis of bacterial communities in the midguts of Apis mellifera and Apis cerana honey bees in Thailand. FEMS Microbiol. Ecol. 79:273–281
17. Engel, P., V.G. Martinson, and N.A. Moran. 2012. Functional diversity within the simple gut microbiota of the honey bee. Proc. Natl. Acad. Sci. U.S.A. 109:11002–11007
18. Engel, P., W.K. Kwong, and N.A. Moran. 2013. Frischella perrara gen. nov., sp. nov., a gammaproteobacterium isolated from the gut of the honey bee, Apis mellifera. Int. J. Syst. Evol. Microbiol. 63:3646–3651
19. Engel, P., and N.A. Moran. 2013. Functional and evolutionary insights into the simple yet specific gut microbiota of the honey bee from metagenomic analysis. Gut Microbes 4:60–65
20. Evans, J.D., and T.N. Armstrong. 2006. Antagonistic interactions between honey bee bacterial symbionts and implications for disease. BMC Ecol. 6:4
21. Gavini, F., J. Mergaert, A. Beji, C. Mielcarek, D. Izard, K. Kersters, and J. De Ley. 1989. Transfer of Enterobacter agglomerans (Beijerinck 1888) Ewing and Fife 1972 to Pantoea gen. nov. as Pantoea agglornerans comb. nov. and description of Pantoea dispersa sp. nov. Int. J. Syst. Evol. Mircobiol. 337–345
22. Hamdi, C., A. Balloi, J. Essanaa, et al. 2011. Gut microbiome dysbiosis and honeybee health. J. Appl. Entomol. 135:524–533
23. Hatjina, F., C. Costa, R. Büchler, et al. 2014. Population dynamics of European honey bee genotypes under different environmental conditions. J. Apicult. Res. 53:233–247
24. Hildebrandt, M.A., C. Hoffmann, S.A. Sherrill-Mix, S.A. Keilbaugh, M. Hamady, Y.Y. Chen, R. Knight, R.S. Ahima, F. Bushman, and G.D. Wu. 2009. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137:1716–1724. e1711–1712
25. Ihrig, J., R. Lill, and U. Mühlenhoff. 2006. Application of the DNAspecific dye EvaGreen for the routine quantification of DNA in microplates. Anal. Biochem. 359:265–267
26. Jeyaprakash, A., M.A. Hoy, and M.H. Allsopp. 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
27. Klungness, L.M.P.Y. 1984. A histochemical study of pollen digestion in the alimentary canal of honeybees (Apis mellifera L.). J. insect. Physiol. 30:511–521
28. Koch, H., and P. Schmid-Hempel. 2011. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc. Natl. Acad. Sci. U.S.A. 108:19288–19292
29. Koch, H., D.P. Abrol, J. Li, and P. Schmid-Hempel. 2013. Diversity and evolutionary patterns of bacterial gut associates of corbiculate bees. Mol. Ecol. 22:2028–2044
30. Kubista, M., J.M. Andrade, M. Bengtsson, et al. 2006. The real-time polymerase chain reaction. Mol. Aspects. Med. 27:95–125
31. Kwong, W.K., and N.A. Moran. 2013. Cultivation and characterization of the gut symbionts of honey bees and bumble bees: Snodgrassella alvi gen. nov., sp. nov., a member of the Neisseriaceae family of the Betaproteobacteria; and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the Enterobacteriales order of the Gammaproteobacteria. Int. J. Syst. Evol. Microbiol. 63:2008–2018
32. Kwong, W.K., P. Engel, H. Koch, and N.A. Moran. 2014. Genomics and host specialization of honey bee and bumble bee gut symbionts. Proc. Natl. Acad. Sci. U.S.A. 111:11509–11514
33. Mao, F., W.Y. Leung, and X. Xin. 2007. Characterization of EvaGreen and the implication of its physicochemical properties for qPCR applications. BMC Biotechnol. 7:76
34. Martinson, V.G., B.N. Danforth, R.L. Minckley, O. Rueppell, S. Tingek, and N.A. Moran. 2011. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol. Ecol. 20:619–628
35. Martinson, V.G., J. Moy, and N.A. Moran. 2012. Establishment of characteristic gut bacteria during development of the honeybee worker. Appl. Environ. Microbiol. 78:2830–2840
36. Mattila, H.R., J. Harris, and G.W. Otis. 2001. Timing production winterbees in honey bee (Apis mellifera) colonies. Insectes Soc. 48:88–93
37. Moran, N.A., A.K. Hansen, J.E. Powell, and Z.L. Sabree. 2012. Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS One 7:e36393
38. Nadkarni, M.A., F.E. Martin, N.A. Jacques, and N. Hunter. 2002. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:257–266
39. Naseribafrouei, A., K. Hestad, E. Avershina, M. Sekelja, A. Linlokken, R. Wilson, and K. Rudi. 2014. Correlation between the human fecal microbiota and depression. Neurogastroenterol. Motil. 26:1155–1162
40. Omholt, S.W. 1987. Thermoregulation in the winter cluster of the honeybee, Apis Mellifera. J. Theor. Biol. 128:219–231
41. Powell, J.E., V.G. Martinson, K. Urban-Mead, and N.A. Moran. 2014. Routes of acquisition of the gut microbiota of Apis mellifera. Appl. Environ. Microbiol. 80:7378–7387
42. Ruijter, J.M., C. Ramakers, W.M. Hoogaars, Y. Karlen, O. Bakker, M.J. van den Hoff, and A.F. Moorman. 2009. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic. Acids. Res. 37:e45
43. Seeley, D.T. 1995. The foraging abilities of a colony, p. 295–307. In The Wisdom of the Hive, the Social and Physiology of the Honey Bee Colonies, First ed. Harvard University Press, Cambridge, Massachusetts London, England.
44. Sekelja, M., I. Rud, S.H. Knutsen, V. Denstadli, B. Westereng, T. Naes, and K. Rudi. 2012. Abrupt temporal fluctuations in the chicken fecal microbiota are explained by its gastrointestinal origin. Appl. Environ. Microbiol. 78:2941–2948
45. Singer, V.L., L.J. Jones, S.T. Yue, and R.P. Haugland. 1997. Characterization of PicoGreen reagent and development of a fluorescence-based solution assay for double-stranded DNA quantitation. Anal. Biochem. 249:228–238
46. Ståhlberg, A., N. Zoric, P. Åman, and M. Kubista. 2005. Quantitative real-time PCR for cancer detection: the lymphoma case. Expert Rev. Mol. Diagn. 5:221–230
47. Taylor, L.P.H.P. 1997. Pollen germination and tube growth. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:461–491
48. Tellam, R.L. 1996. The peritrophic matrix., p. 86–114, In M.J.Lehane and P.F. Billingsley (ed.), Biology of the Insect Midgut. Chapman & Hall, London.
49. Trosvik, P., B. Skånseng, K.S. Jakobsen, N.C. Stenseth, T. Næs, and K. Rudi. 2007. Multivariate analysis of complex DNA sequence electropherograms for high-throughput quantitative analysis of mixed microbial populations. Appl. Environ. Microbiol. 73:4975–4983
50. Trosvik, P., K. Rudi, T. Naes, A. Kohler, K.S. Chan, K.S. Jakobsen, and N.C. Stenseth. 2008. Characterizing mixed microbial population dynamics using time-series analysis. ISME J. 2:707–715
51. vanEngelsdorp, D., and M.D. Meixner. 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
52. Vasquez, A., E. Forsgren, I. Fries, R.J. Paxton, E. Flaberg, L. Szekely, and T.C. Olofsson. 2012. Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS One 7:e33188
53. Wu, M., Y. Sugimura, N. Takaya, D. Takamatsu, M. Kobayashi, D. Taylor, and M. Yoshiyama. 2013. Characterization of bifidobacteria in the digestive tract of the Japanese honeybee, Apis cerana japonica. J. Invertebr. Pathol. 112:88–93
54. Yoshiyama, M., and K. Kimura. 2009. Bacteria in the gut of Japanese honeybee, Apis cerana japonica, and their antagonistic effect against Paenibacillus larvae, the causal agent of American foulbrood. J. Invertebr. Pathol. 102:91–96
55. Yu, Y., C. Lee, J. Kim, and S. Hwang. 2005. Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol. Bioeng. 89:670–679
56. Zimonja, M., K. Rudi, P. Trosvik, and T. Næs. 2008. Multivariate curve resolution of mixed bacterial DNA sequence spectra: identification and quantification of bacteria in undefined mixture samples. J. Chemometr. 22:309–322.