16S rRNA amplicon sequencing demonstrates that indoor-reared bumblebees (Bombus terrestris) harbor a core subset of bacteria normally associated with the wild host

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Meeus, Ivan ^a   Parmentier, Laurian ^a   Billiet, Annelies ^a   Maebe, Kevin ^a   Van Nieuwerburgh, Filip ^a   Deforce, Dieter ^a   Wäckers, Felix ^b   Vandamme, Peter ^c   Smagghe, Guy ^a  

^a GHENT UNIVERSITY   (Belgium)

^b Biobest Belgium NV   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S; BACTERIAL RNA;

AMPLICON; ANIMAL TISSUE; ARTICLE; BACTERIUM; BACTERIUM DETECTION; BIFIDOBACTERIACEAE; BIFIDOBACTERIUM; BOMBUS TERRESTRIS; CONTROLLED STUDY; GENE SEQUENCE; INTESTINE FLORA; LACTOBACILLACEAE; LACTOBACILLUS; NEISSERIACEAE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORBACEAE; POPULATION ABUNDANCE; SPECIES DIFFERENCE; WILD SPECIES; WORKER (INSECT); ANIMAL; CLASSIFICATION; GENETICS; HYMENOPTERA; MICROBIOLOGY; MICROFLORA;

BIFIDOBACTERIACEAE; BIFIDOBACTERIUM; BOMBUS TERRESTRIS; ENTEROBACTERIACEAE; LACTOBACILLACEAE; LACTOBACILLUS; NEISSERIACEAE;

ANIMALS; BACTERIA; HYMENOPTERA; MICROBIOTA; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S;

EID: 84928801146     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125152     Document Type: Article

References (51)

1. Goulson D. Bumblebees: Their behaviour and ecology. Goulson D, editor. New York: Oxford university press; 2003.
2. Goulson D, Hanley ME, Darvill B, Ellis JS, Knight ME. Causes of rarity in bumblebees. Biological Conservation. 2005; 122(1):1-8.
3. Velthuis HHW, van Doorn A. A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie. 2006; 37(4):421-51. PMID: 16996085
4. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE. Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol. 2010; 25(6):345-53. doi: 10.1016/j.tree.2010.01.007 PMID: 20188434
5. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemuller R, Edwards M, Peeters T, et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science. 2006; 313(5785):351-4. PMID: 16857940
6. Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, et al. Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci Unit States Am. 2011; 108(2):662-7. doi: 10.1073/pnas.1014743108 PMID: 21199943
7. Winfree R, Aguilar R, Vazquez DP, LeBuhn G, Aizen MA. A meta-analysis of bees' responses to anthropogenic disturbance. Ecology. 2009; 90(8):2068-76. PMID: 19739369
8. Whitehorn PR, O'Connor S, Wackers FL, Goulson D. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science. 2012; 336(6079):351-2. doi: 10.1126/science.1215025 PMID: 22461500
9. Meeus I, Brown MJF, De Graaf DC, Smagghe G. Effects of invasive parasites on bumble bee declines. Conservation Biology. 2011; 25(4):662-71. doi: 10.1111/j.1523-1739.2011.01707.x PMID: 21771075
10. Williams PH, Osborne JL. Bumblebee vulnerability and conservation world-wide. Apidologie. 2009; 40(3):367-87.
11. Brown MJF, Paxton RJ. The conservation of bees: a global perspective. Apidologie. 2009; 40(3):410-6.
12. Hamdi C, Balloi A, Essanaa J, Crotti E, Gonella E, Raddadi N, et al. Gut microbiome dysbiosis and honeybee health. Journal of Applied Entomology. 2011; 135(7):524-33.
13. Cariveau PD, Powell JE, Koch H, Winfree LT, Moran NA. Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). ISME J. 2014 1-11. doi: 10.1038/ismej.2014.99 PMID: 24936764
14. Koch H, Schmid-Hempel P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci USA. 2011; 108(48):19288-92. doi: 10.1073/pnas.1110474108 PMID: 22084077
15. Koch H, Schmid-Hempel P. Bacterial communities in central European cumblebees: low diversity and high specificity. Microb Ecol. 2011; 62(1):121-33. doi: 10.1007/s00248-011-9854-3 PMID: 21556885
16. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol Ecol. 2011; 20(3):619-28. doi: 10.1111/j.1365-294X.2010.04959.x PMID: 21175905
17. Engel P, Moran NA. The gut microbiota of insects-diversity in structure and function. Fems Microbiology Reviews. 2013; 37(5):699-735. doi: 10.1111/1574-6976.12025 PMID: 23692388
18. Parmentier L, Meeus I, Cheroutre L, Mommaerts V, Louwye S, Smagghe G. Commercial bumblebee hives to assess an anthropogenic environment for pollinator support: a case study in the region of Ghent (Belgium). Environ Monit Assess. 2014; 186(4):2357-67. doi: 10.1007/s10661-013-3543-2 PMID: 24297306
19. Meeus I, Mommaerts V, Billiet A, Mosallanejad H, Van de Wiele T, Wackers F, et al. Assessment of mutualism between Bombus terrestris and its microbiota by use of microcolonies. Apidologie. 2013; 44(6):708-19.
20. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108:4516-22. doi: 10.1073/pnas.1000080107 PMID: 20534432
21. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities. Applied and Environmental Microbiology. 2009; 75(23):7537-41. doi: 10.1128/AEM.01541-09 PMID: 19801464
22. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a Dual-Index Sequencing Strategy and Curation Pipeline for Analyzing Amplicon Sequence Data on the MiSeq Illumina Sequencing Platform. Applied and Environmental Microbiology. 2013; 79(17):5112-20. doi: 10.1128/AEM.01043-13 PMID: 23793624
23. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011; 27(16):2194-200. doi: 10.1093/bioinformatics/btr381 PMID: 21700674
24. Newton ILG, Roeselers G. The effect of training set on the classification of honey bee gut microbiota using the Naive Bayesian Classifier. BMC Microbiol. 2012;12. doi: 10.1186/1471-2180-12-12 PMID: 22251616
25. Maebe K, Meeus I, Ganne M, Wackers F, Smagghe G. Scientific note on microsatellite DNA analyses revealing diploid and haploid drones in bumblebee mass breeding. Apidologie. 2014; 45(2):189-91.
26. Maebe K, Meeus I, Maharramov J, Grootaert P, Michez D, Rasmont P, et al. Microsatellite analysis in museum samples reveals inbreeding before the regression of Bombus veteranus. Apidologie. 2013; 44(2):188-97.
27. Wang JL. Sibship reconstruction from genetic data with typing errors. Genetics. 2004; 166(4):1963-79. PMID: 15126412
28. Mulder CPH, Bazeley-White E, Dimitrakopoulos PG, Hector A, Scherer-Lorenzen M, Schmid B. Species evenness and productivity in experimental plant communities. Oikos. 2004; 107(1):50-63.
29. Pielou EC. Measurement of Diversity in Different Types of Biological Collections. Journal of Theoretical Biology. 1966; 13(Dec):131-&.
30. Warton DI, Wright ST, Wang Y. Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution. 2012; 3(1):89-101.
31. Warton DI. Many zeros does not mean zero inflation: comparing the goodness-of-fit of parametric models to multivariate abundance data. Environmetrics. 2005; 16(3):275-89.
32. Wang Y, Naumann U, Wright ST, Warton DI. mvabund- an R package for model-based analysis of multivariate abundance data. Methods in Ecology and Evolution. 2012; 3(3):471-4.
33. Warton DI. Raw data graphing: an informative but under-utilized tool for the analysis of multivariate abundances. Austral Ecology. 2008; 33(3):290-300.
34. Moran NA, Hansen AK, Powell JE, Sabree ZL. Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS ONE. 2012; 7(4):e36393 doi: 10.1371/journal.pone.0036393 PMID: 22558460
35. Mohr KI, Tebbe CC. Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environ Microbiol. 2006; 8(2):258-72. PMID: 16423014
36. Behar A, Yuval B, Jurkevitch E. Enterobacteria-mediated nitrogen fixation in natural populations of the fruit fly Ceratitis capitata. Mol Ecol. 2005; 14(9):2637-43. PMID: 16029466
37. Demirci M, Sevim E, Demir I, Sevim A. Culturable bacterial microbiota of Plagiodera versicolora (L.) (Coleoptera: Chrysomelidae) and virulence of the isolated strains. Folia Microbiologica. 2013; 58(3):201-10. doi: 10.1007/s12223-012-0199-1 PMID: 23054688
38. Podgwaite JD, D'Amico V, Zerillo RT, Schoenfeldt H. Bacteria Associated with Larvae and Adults of the Asian Longhorned Beetle (Coleoptera: Cerambycidae). J Entomol Sci. 2013; 48(2):128-38.
39. Vasanthakumar A, Delalibera I, Handelsman J, Klepzig KD, Schloss PD, Raffa KF. Characterization of gut-associated bacteria in larvae and adults of the southern pine beetle, Dendroctonus frontalis Zimmermann. Environ Entomol. 2006; 35(6):1710-7.
40. Koch H, Abrol DP, Li JL, Schmid-Hempel P. Diversity and evolutionary patterns of bacterial gut associates of corbiculate bees. Mol Ecol. 2013; 22(7):2028-44. doi: 10.1111/mec.12209 PMID: 23347062
41. Pridal P, Sedlácek L, Marvanová L. Microbiology of Bombus terrestris L. larvae (Hymenoptera: Apoidea) from laboratory rearing. Acta univ agric et silvic Mendel Brun 1997; 8:59-66.
42. Fürst MA, McMahon DP, Osborne JL, Paxton RJ, Brown MJF. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature. 2014; 506(7488):364-+. doi: 10.1038/nature12977 PMID: 24553241
43. Murray TE, Coffey MF, Kehoe E, Horgan FG. Pathogen prevalence in commercially reared bumble bees and evidence of spillover in conspecific populations. Biol Conservat. 2013; 159:269-76.
44. Meeus I, Brown MJF, De Graaf DC, Smagghe G. Effects of invasive parasites on bumble bee declines. Conservat Biol. 2011; 25(4):662-71.
45. Ventura M, Turroni F, Motherway MO, MacSharry J, van Sinderen D. Host-microbe interactions that facilitate gut colonization by commensal bifidobacteria. Trends in Microbiology. 2012; 20(10):467-76. doi: 10.1016/j.tim.2012.07.002 PMID: 22902802
46. Engel P, Martinson VG, Moran NA. Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci USA. 2012; 109(27):11002-7. doi: 10.1073/pnas.1202970109 PMID: 22711827
47. Babendreier D, Joller D, Romeis J, Bigler F, Widmer F. Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol Ecol. 2007; 59(3):600-10. PMID: 17381517
48. Engel P, Kwong WK, Moran NA. Frischella perrara gen. nov., sp nov., a gammaproteobacterium isolated from the gut of the honeybee, Apis mellifera. Int J Syst Evol Microbiol. 2013; 63:3646-51. doi: 10.1099/ijs.0.049569-0 PMID: 23606484
49. Mohr KI, Tebbe CC. Field study results on the probability and risk of a horizontal gene transfer from transgenic herbicide-resistant oilseed rape pollen to gut bacteria of bees. Appl Microbiol Biotechnol. 2007; 75(3):573-82. PMID: 17273854
50. Killer J, Kopecny J, Mrazek J, Koppova I, Havlik J, Benada O, et al. Bifidobacterium actinocoloniiforme sp nov and Bifidobacterium bohemicum sp nov., from the bumblebee digestive tract. Int J Syst Evol Microbiol. 2011; 61:1315-21. doi: 10.1099/ijs.0.022525-0 PMID: 20656822
51. Killer J, Kopecny J, Mrazek J, Rada V, Dubna S, Marounek M. Bifidobacteria in the digestive tract of bumblebees. Anaerobe. 2010; 16(2):165-70. doi: 10.1016/j.anaerobe.2009.07.007 PMID: 19651224