Deep sequencing and ecological characterization of gut microbial communities of diverse bumble bee species

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Lim, Haw Chuan ^a,b   Chu, Chia Ching ^a   Seufferheld, Manfredo J ^a   Cameron, Sydney A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b DEPARTMENT OF PALEOBIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINOBACTERIA; ALPHAPROTEOBACTERIA; ARTICLE; BACILLI; BETAPROTEOBACTERIA; BIOFILM; BOMBUS ATRATUS; BOMBUS BOHEMICUS; BOMBUS CONVEXUS; BOMBUS FRATERNUS; BOMBUS IMPATIENS; BOMBUS PENSYLVANICUS; BOMBUS TERRESTRIS; BOMBUS TERRICOLA; BOMBUS USSURENSIS; BUMBLEBEE; COMMUNITY FINGERPRINTING; COMMUNITY STRUCTURE; CONTROLLED STUDY; FLAVOBACTERIA; FLUORESCENCE MICROSCOPY; GAMMAPROTEOBACTERIA; GENETIC ENGINEERING; GEOGRAPHY; INTESTINE FLORA; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; NONHUMAN; OPERATIONAL TAXONOMIC UNIT; PHYLOGENY; PYROSEQUENCING; SNODGRASSELLA ALVI; TAXONOMY; ANIMAL; BACTERIUM; BEE; ECOLOGY; GASTROINTESTINAL TRACT; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; MICROBIOLOGY; PROCEDURES; SEQUENCE ANALYSIS; SYMBIOSIS;

ACTINOBACTERIA; ALPHAPROTEOBACTERIA; APIS MELLIFERA; APOIDEA; BACILLI (CLASS); BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; BOMBUS (GENUS); FLAVOBACTERIA; GAMMAPROTEOBACTERIA; OTUS;

RNA 16S;

ANIMALS; BACTERIA; BEES; BIOFILMS; ECOLOGY; GASTROINTESTINAL TRACT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS; SYMBIOSIS;

EID: 84928911068     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118566     Document Type: Article

References (76)

1. Fraune S, Bosch TCG (2010) Why bacteria matter in animal development and evolution. BioEssays 32: 571-580. doi: 10.1002/bies.200900192 PMID: 20544735
2. Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9: 313-323. doi: 10.1038/nri2515 PMID: 19343057
3. Gil R, Sabater-Munoz B, Latorre A, Silva FJ, Moya A (2002) Extreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life. Proc Natl Acad Sci USA 99: 4454-4458. PMID: 11904373
4. Warnecke F, Luginbuhl P, Ivanova N, Ghassemian M, Richardson TH, et al. (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450: 560-565. PMID: 18033299
5. Rolfe RD (1997) Colonization resistance. In: Mackie RI, White B.A. and Isaacson R.E., editor. Gastrointestinal microbiology. London: Chapman and Hall. pp. 501-536.
6. Reid G, Howard J, Gan BS (2001) Can bacterial interference prevent infection? Trends Microbiol 9: 424-428. PMID: 11553454
7. King JG, Hillyer JF (2012) Infection-induced interaction between the mosquito circulatory and immune systems. PLoS Pathog 8: e1003058. doi: 10.1371/journal.ppat.1003058 PMID: 23209421
8. Greenberg B, Kowalski JA, Klowden MJ (1970) Factors affecting the transmission of Salmonella by flies: Natural resistance to colonization and bacterial interference. Infect Immun 2: 800-809. PMID: 16557919
9. Jarosz J (1979) Gut flora of Galleria mellonella suppressing ingested bacteria. J Invertebr Pathol 34: 192-198. PMID: 119813
10. Veivers PC, O'Brien RW, Slaytor M (1982) Role of bacteria in maintaining the redox potential in the hindgut of termites and preventing entry of foreign bacteria. J Insect Physiol 28: 947-951.
11. Dillon RJ, Charnley AK (1986) Inhibition of Metarhizium anisopliae by the gut bacterial flora of the desert locust, Schistocerca gregaria: Evidence for an antifungal toxin. J Invertebr Pathol 47: 350-360.
12. Koch H, Schmid-Hempel P (2011) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci USA 108: 19288-19292. doi: 10.1073/pnas.1110474108 PMID: 22084077
13. 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. PMID: 14615218
14. Mohr KI, Tebbe CC (2006) Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environ Microbiol 8: 258-272. PMID: 16423014
15. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, et al. (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Mol Ecol 20: 619-628. doi: 10.1111/j.1365-294X.2010.04959.x PMID: 21175905
16. Anderson KE, Sheehan TH, Eckholm BJ, Mott BM, DeGrandi-Hoffman G (2011) An emerging paradigm of colony health: Microbial balance of the honey bee and hive (Apis mellifera). Insectes Soc 58: 431-444.
17. Engel P, Martinson VG, Moran NA (2012) Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci USA 109: 11002-11007. doi: 10.1073/pnas.1202970109 PMID: 22711827
18. Koch H, Schmid-Hempel P (2012) Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host-parasite system. Ecol Lett 15: 1095-1103. doi: 10.1111/j.1461-0248.2012.01831.x PMID: 22765311
19. Vasquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, et al. (2012) Symbionts as major modulators of insect health: Lactic acid bacteria and honeybees. PLoS ONE 7: e33188. doi: 10.1371/journal.pone.0033188 PMID: 22427985
20. Koch H, Cisarovsky G, Schmid-Hempel P (2012) Ecological effects on gut bacterial communities in wild bumblebee colonies. J Anim Ecol 81: 1202-1210. doi: 10.1111/j.1365-2656.2012.02004.x PMID: 22708631
21. Babendreier D, Joller D, Romeis J, Bigler F, Widmer F (2007) Bacterial community structures in honey-bee intestines and their response to two insecticidal proteins. FEMS Microbiol Ecol 59: 600-610. PMID: 17381517
22. Klee J, Besana AM, Genersch E, Gisder S, Nanetti A, et al. (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol 96: 1-10. PMID: 17428493
23. Cox-Foster DL, Conlan S, Holmes EC, Palacios G, Evans JD, et al. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318: 283-287. PMID: 17823314
24. Sammataro D, Gerson U, Needham G (2000) Parasitic mites of honey bees: Life history, implications, and impact. Annu Rev Entomol 45: 519-548. PMID: 10761588
25. Genersch E (2010) American foulbrood in honeybees and its causative agent, Paenibacillus larvae. J Invertebr Pathol 103, Supplement: S10-S19. doi: 10.1016/j.jip.2009.06.015 PMID: 19909971
26. Whitehorn PR, O'Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336: 351-352. doi: 10.1126/science.1215025 PMID: 22461500
27. Henry M, Béguin M, Requier F, Rollin O, Odoux J-F, et al. (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336: 348-350. doi: 10.1126/science.1215039 PMID: 22461498
28. Brown MJF, Paxton RJ (2009) The conservation of bees: A global perspective. Apidologie 40: 410-416.
29. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, et al. Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25: 345-353. doi: 10.1016/j.tree.2010.01.007 PMID: 20188434
30. Alaux C, Brunet J-L, Dussaubat C, Mondet F, Tchamitchan S, et al. (2010) Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ Microbiol 12: 774-782. doi: 10.1111/j.1462-2920.2009.02123.x PMID: 20050872
31. Bromenshenk JJ, Henderson CB, Wick CH, Stanford MF, Zulich AW, et al. (2010) Iridovirus and microsporidian linked to honey bee colony decline. PLoS ONE 5: e13181. doi: 10.1371/journal.pone.0013181 PMID: 20949138
32. Koch H, Abrol DP, Li J, Schmid-Hempel P (2013) Diversity and evolutionary patterns of bacterial gut associates of corbiculate bees. Mol Ecol 22: 2028-2044. doi: 10.1111/mec.12209 PMID: 23347062
33. Koch H, Schmid-Hempel P (2011) Bacterial communities in Central European Bumblebees: Low diversity and high specificity. Microb Ecol 62: 121-133. doi: 10.1007/s00248-011-9854-3 PMID: 21556885
34. Martinson VG, Moy J, Moran NA (2012) Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol 78: 2830-2840. doi: 10.1128/AEM.07810-11 PMID: 22307297
35. Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, et al. (2011) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci USA 108: 662-667. doi: 10.1073/pnas.1014743108 PMID: 21199943
36. Grixti JC, Wong LT, Cameron SA, Favret C (2009) Decline of bumble bees (Bombus) in the North American Midwest. Biol Conserv 142: 75-84.
37. Cameron SA, Hines HM, Williams PH (2007) A comprehensive phylogeny of the bumble bees (Bombus). Biol J Linn Soc 91: 161-188.
38. Wang Y, Qian P-Y (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS ONE 4: e7401. doi: 10.1371/journal.pone.0007401 PMID: 19816594
39. Liu ZZ, DeSantis TZ, Andersen GL, Knight R (2008) Accurate taxonomy assignments from 16S rRNA sequences produced by highly parallel pyrosequencers. Nucleic Acids Res 36.
40. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267. PMID: 17586664
41. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, et al. (2009) Introducing mothur: Opensource, platform-Independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541. doi: 10.1128/AEM.01541-09 PMID: 19801464
42. Newton I, Roeselers G (2012) The effect of training set on the classification of honey bee gut microbiota using the Naive Bayesian Classifier. BMC Microbiol 12: 221. doi: 10.1186/1471-2180-12-221 PMID: 23013113
43. Ozer S, Xu W, Gardner DP, Miranker DP, Gutell RR, et al. (2012) An accurate scalable template-based alignment algorithm. Proceedings of the 2012 IEEE International Conference on Bioinformatics and Biomedicine (BIBM): IEEE Computer Society.
44. Bernhart SH, Hofacker IL, Will S, Gruber AR, Stadler PF (2008) RNAalifold: Improved consensus structure prediction for RNA alignments. BMC Bioinformatics 9: 474. doi: 10.1186/1471-2105-9-474 PMID: 19014431
45. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61: 539-542. doi: 10.1093/sysbio/sys029 PMID: 22357727
46. Liu Z, Lozupone C, Hamady M, Bushman FD, Knight R (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35: e120. PMID: 17881377
47. Lozupone C, Knight R (2005) UniFrac: A new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235. PMID: 16332807
48. Lozupone C, Hamady M, Knight R (2006) UniFrac - An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 7: 371. PMID: 16893466
49. Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65: 4630-4636. PMID: 10508099
50. Cardinale M, Brusetti L, Quatrini P, Borin S, Puglia AM, et al. (2004) Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities. Appl Environ Microbiol 70: 6147-6156. PMID: 15466561
51. Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H, Buckley DH (2009) T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinformatics 10: 171. doi: 10.1186/1471-2105-10-171 PMID: 19500385
52. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271-280.
53. Oksanen J, Blanchet FG, Kindt R, Legendre P, O'Hara RB, et al. (2011) Vegan: Community ecology package: R package version 1.17-9. http://CRAN.R-project.org/package = vegan.
54. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA for PRIMER: Guide to software and statistical methods. Plymouth, United Kingdom: PRIMER-E
55. Humayoun SB, Bano N, Hollibaugh JT (2003) Depth distribution of microbial diversity in Mono Lake, a meromictic soda lake in California. Appl Environ Microbiol 69: 1030-1042. PMID: 12571026
56. Endo A, Irisawa T, Futagawa-Endo Y, Sonomoto K, Itoh K, et al. (2010) Fructobacillus tropaeoli sp. nov., a fructophilic lactic acid bacterium isolated from a flower. Int J Syst Evol Microbiol 61: 898-902. doi: 10.1099/ijs.0.023838-0 PMID: 20495031
57. Jojima Y, Mihara Y, Suzuki S, Yokozeki K, Yamanaka S, et al. (2004) Saccharibacter floricola gen. nov., sp. nov., a novel osmophilic acetic acid bacterium isolated from pollen. Int J Syst Evol Microbiol 54: 2263-2267. PMID: 15545468
58. Edwards CG, Haag KM, Collins MD, Hutson RA, Huang YC (1998) Lactobacillus kunkeei sp. nov.: a spoilage organism associated with grape juice fermentations. J Appl Microbiol 84: 698-702. PMID: 9674120
59. Anderson KE, Sheehan TH, Mott BM, Maes P, Snyder L, et al. (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. doi: 10.1371/journal.pone.0083125 PMID: 24358254
60. McFrederick QS, Wcislo WT, Taylor DR, Ishak HD, Dowd SE, et al. (2012) Environment or kin: Whence do bees obtain acidophilic bacteria? Mol Ecol 21: 1754-1768. doi: 10.1111/j.1365-294X.2012.05496.x PMID: 22340254
61. Aizenberg-Gershtein Y, Izhaki I, Halpern M (2013) Do honeybees shape the bacterial community composition in floral nectar? PLoS ONE 8: e67556. doi: 10.1371/journal.pone.0067556 PMID: 23844027
62. Fridman S, Izhaki I, Gerchman Y, Halpern M (2011) Bacterial communities in floral nectar. Environ Microbiol Rep 4: 97-104. doi: 10.1111/j.1758-2229.2011.00309.x PMID: 23757235
63. Shade A, McManus PS, Handelsman J (2013) Unexpected diversity during community succession in the apple flower microbiome. mBio 4.
64. Torretta JP, Medan D, Abrahamovich AH (2006) First record of the invasive bumblebee Bombus terrestris (L.) (Hymenoptera, Apidae) in Argentina. Trans Am Entomol Soc 132: 285-289.
65. Morales CL, Arbetman MP, Cameron SA, Aizen MA (2013) Rapid ecological replacement of a native bumble bee by invasive species. Front Ecol Environ 11: 529-534.
66. Vásquez A, Olofsson TC (2009) The lactic acid bacteria involved in the production of bee pollen and bee bread. J Apic Res 48: 189-195.
67. Gilliam M (1997) Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiol Lett 155: 1-10.
68. Michener CD, Winston ML, Jander R (1978) Pollen manipulation and related activities and structures in bees of the family Apidae. Univ Kansas Sci Bull 51: 575-601.
69. Forsgren E, Olofsson T, Vasquez A, Fries I (2010) Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41: 99-108.
70. Evans J, Armstrong T-N (2006) Antagonistic interactions between honey bee bacterial symbionts and implications for disease. BMC Ecol 6: 4. PMID: 16551367
71. Arbetman M, Meeus I, Morales C, Aizen M, Smagghe G (2013) Alien parasite hitchhikes to Patagonia on invasive bumblebee. Biol Invasions 15: 489-494.
72. Maharramov J, Meeus I, Maebe K, Arbetman M, Morales C, et al. (2013) Genetic variability of the neogregarine Apicystis bombi, an etiological agent of an emergent bumblebee disease. PLoS ONE 8: e81475. doi: 10.1371/journal.pone.0081475 PMID: 24324696
73. Mao W, Schuler MA, Berenbaum MR (2013) Honey constituents up-regulate detoxification and immunity genes in the western honey bee Apis mellifera. Proc Natl Acad Sci USA 110: 8842-8846. doi: 10.1073/pnas.1303884110 PMID: 23630255
74. Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, et al. (2010) 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol 188: 291-301. doi: 10.1111/j.1469-8137.2010.03373.x PMID: 20636324
75. Lukjancenko O, Wassenaar T, Ussery D (2010) Comparison of 61 sequenced Escherichia coli genomes. Microb Ecol 60: 708-720. doi: 10.1007/s00248-010-9717-3 PMID: 20623278
76. Kwong WK, Moran NA (2013) 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. Int J Syst Evol Microbiol 63: 2008-2018. doi: 10.1099/ijs.0.044875-0 PMID: 23041637