Establishment of characteristic gut bacteria during development of the honeybee worker

Applied and Environmental Microbiology

Volumn 78, Issue 8, 2012, Pages 2830-2840

  Martinson, Vincent G ^a   Moy, Jamie ^b   Moran, Nancy A ^b,c  

^a UNIVERSITY OF ARIZONA   (United States)

^b University of Arizona   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE; APIS MELLIFERA; FLUORESCENT IN SITU HYBRIDIZATION; FOOD SOURCES; GUT BACTERIA; MICROBIOTAS; PHYLOTYPES; QUANTITATIVE PCR;

GENES; POLYMERASE CHAIN REACTION; RNA;

BACTERIA;

BACTERIAL DNA; RIBOSOME DNA; RNA 16S;

ABUNDANCE; BACTERIUM; COLONIZATION; HONEYBEE; IN SITU MEASUREMENT; INTERSPECIFIC VARIATION; LIFE CYCLE; MICROBIAL COMMUNITY; SPATIAL DISTRIBUTION;

ANIMAL; ARTICLE; BACTERIUM; BEE; BIODIVERSITY; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; FECES; FLUORESCENCE IN SITU HYBRIDIZATION; GASTROINTESTINAL TRACT; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; BACTERIA; BEES; BIODIVERSITY; CLUSTER ANALYSIS; DNA, BACTERIAL; DNA, RIBOSOMAL; FECES; GASTROINTESTINAL TRACT; IN SITU HYBRIDIZATION, FLUORESCENCE; MOLECULAR SEQUENCE DATA; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

APIS MELLIFERA; APOIDEA;

EID: 84860462269     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.07810-11     Document Type: Article

References (63)

1. Ament SA, Corona M, Pollock HS, Robinson GE. 2008. Insulin signaling is involved in the regulation of worker division of labor in honey bee colonies. Proc. Natl. Acad. Sci. U. S. A. 105:4226-4231.
2. Babendreier D, Joller D, Romeis J, Bigler F, Widmer F. 2007. Bacterial community structures in honeybee intestines and their response to two insecticidal proteins. FEMS Microbiol. Ecol. 59:600-610.
3. Brune A, Friedrich M. 2000. Microecology of the termite gut: structure and function on a microscale. Curr. Opin. Microbiol. 3:263-269.
4. Caporaso JG, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335-336.
5. Chapman RF. 1998. The insects: structure and function, 4th ed. Cambridge University Press, Cambridge, United Kingdom.
6. Cole JR, et al. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141- D145.
7. Cox-Foster DL, et al. 2007. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318:283-287.
8. Cremer S, Armitage SAO, Schmid-Hempel P. 2007. Social immunity. Curr. Biol. 17:R693-R702.
9. Cremer S, Sixt M. 2009. Analogies in the evolution of individual and social immunity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364:129 -142.
10. Cruz-Landim C, Rodrigues L. 1967. Comparative anatomy and histology of the alimentary canal of adult Apinae. J. Apicult. Res. 6:17-28.
11. Daims H, Stoecker K, Wagner M. 2005. Fluorescent in situ hybridization for the detection of prokaryotes. In Osborn AM, Smith CJ (ed.), Molecular microbial ecology. Taylor & Francis Group, New York, NY.
12. Dillon RJ, Dillon VM. 2004. The gut bacteria of insects: nonpathogenic interactions. Annu. Rev. Entomol. 49:71-92.
13. Evans JD, Chen YP, Di Prisco G, Pettis J, Williams V. 2009. Bee cups: single-use cages for honey bee experiments. J. Apicult. Res. 48:300 -302.
14. Evans JD, Lopez DL. 2004. Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). J. Econ. Entomol. 97: 752-756.
15. Forsgren E. 2010. European foulbrood in honey bees. J. Invertebr. Pathol. 103:S5-S9.
16. Forsgren E, Olofsson TC, Vasquez A, Fries I. 2011. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41:99 -108.
17. Gilliam M. 1997. Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiol. Lett. 155:1-10.
18. Gilliam M. 1971. Microbial sterility of the intestinal content of the immature honey bee, Apis mellifera. Ann. Entomol. Soc. Am. 64:315-316.
19. Gilliam M, Prest DB. 1987. Microbiology of feces of the larval honey bee, Apis mellifera. J. Invertebr. Pathol. 49:70 -75.
20. Hammer O, Harper DAT. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4:1-9.
21. Haydak MH. 1970. Honey bee nutrition. Annu. Rev. Entomol. 15:143- 156.
22. Hongoh Y, et al. 2005. Intra- and interspecific comparisons of bacterial diversity and community structure support coevolution of gut microbiota and termite host. Appl. Environ. Microbiol. 71:6590-6599.
23. Hongoh Y, et al. 2006. Intracolony variation of bacterial gut microbiota among castes and ages in the fungus-growing termite Macrotermes gilvus. Mol. Ecol. 15:505-516.
24. Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T. 2006. Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biol. 4:1841-1851.
25. 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.
26. Jimenez DR, Gilliam M. 1996. Peroxisomal enzymes in the honey bee midgut. Arch. Insect Biochem. Physiol. 31:87-103.
27. Kaltenpoth M, Goettler W, Koehler S, Strohm E. 2010. Life cycle and population dynamics of a protective insect symbiont reveal severe bottlenecks during vertical transmission. Evol. Ecol. 24:463- 477.
28. Kikuchi Y, Hosokawa T, Fukatsu T. 2007. Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl. Environ. Microbiol. 73:4308-4316.
29. Klein AM, et al. 2007. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274:303-313.
30. Koch H, Schmid-Hempel P. 2011. Bacterial communities in central European bumblebees: low diversity and high specificity. Microb. Ecol. 62: 121-133.
31. Koch H, Schmid-Hempel P. 2011. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc. Natl. Acad. Sci. U. S. A. doi:10.1073/pnas.1110474108.
32. Lee YK, Mazmanian SK. 2010. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330:1768 -1773.
33. Ley RE, et al. 2008. Evolution of mammals and their gut microbes. Science 320:1647-1651.
34. Martinson VG, et al. 2011. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol. Ecol. 20:619-628.
35. Maurizio A. 1975. How bees make honey, p. 197-220. In E. Crane (ed.), Honey, a comprehensive study, vol. 72. Heinemann, London, United Kingdom.
36. 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.
37. Mohr KI, Tebbe CC. 2007. 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. Biot. 75:573-582.
38. Ochman H, et al. 2010. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biol. 8:e1000546.
39. Oliver KM, Moran NA, Hunter MS. 2006. Costs and benefits of a superinfection of facultative symbionts in aphids. Proc. R. Soc. B 273:1273- 1280.
40. Olofsson TC, Vasquez A. 2008. Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Curr. Microbiol. 57:356 -363.
41. Robinson CJ, Schloss P, Ramos Y, Raffa K, Handelsman J. 2010. Robustness of the bacterial community in the cabbage white butterfly larval midgut. Microb. Ecol. 59:199 -211.
42. Roulston TH, Cane JH. 2000. Pollen nutritional content and digestibility for animals. Plant Syst. Evol. 222:187-209.
43. Round JL, Mazmanian SK. 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9:313- 323.
44. Sammataro D, Cicero JM. 2010. Functional morphology of the honey stomach wall of the European honey bee (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 103:979 -987.
45. Santos CG, Serrao JE. 2006. Histology of the ileum in bees (Hymenoptera, Apoidea). Braz. J. Morphol. Sci. 23:405- 413.
46. Schloss PD, et al. 2009. Introducing mothur: open-source, platformindependent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541.
47. Schmid-Hempel P. 1998. Parasites in social insects. Princeton University Press, Princeton, NJ.
48. Seeley TD. 1982. Adaptive significance of the age polythism schedule in honeybee colonies. Behav. Ecol. Sociobiol. 11:287-293.
49. Seeley TD. 1985. Honeybee ecology. Princeton University Press, Princeton, NJ.
50. Shimanuki H, Knox DA. 2000. Diagnosis of honey bee diseases. Agriculture handbook no. AH-690. USDA, Washington, DC.
51. Snodgrass RE. 1910. The anatomy of the honey bee. Government Printing Office, Washington, DC.
52. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688 -2690.
53. Tellam RL. 1996. The peritrophic matrix, p. 86 -114. In Lehane MJ, Billingsley PF (ed.), Biology of the insect midgut. Chapman & Hall, London, United Kingdom.
54. Terra WR, Ferreira C, Baker JE. 1996. Compartmentalization of digestion, p. 206-235. In Lehane MJ, Billingsley PF (ed.), Biology of the insect midgut. Chapman & Hall, London, United Kingdom.
55. U'Ren JM, Lutzoni F, Miadlikowska J, Arnold AE. 2010. Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microb. Ecol. 60:340 -353.
56. Vane-Wright RI, Raheem DC, Cieslak A, Vogler AP. 1999. Evolution of the mimetic African swallowtail butterfly Papilio dardanus: molecular data confirm relationships with P. phorcas and P. constantinus. Biol. J. Linnean Soc. 66:215-229.
57. Vasquez A, Olofsson TC. 2009. The lactic acid bacteria involved in the production of bee pollen and bee bread. J. Apicult. Res. 48:189 -195.
58. Warnecke F, et al. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560 -565.
59. Weston RJ. 2000. The contribution of catalase and other natural products to the antibacterial activity of honey: a review. Food Chem. 71:235-239.
60. White JW, Schepartz AI, Subers MH. 1963. The identification of inhibine, the antibacterial factor in honey, as hydrogen peroxide and its origin in a honey glucose-oxidase system. Biochim. Biophys. Acta 73:57-70.
61. Wilson E. 2000. Sociobiology: the new synthesis. Harvard University Press, Cambridge, MA.
62. Winston ML. 1985. The biology of the honey bee. Harvard University Press, Cambridge, MA.
63. Yue D, Nordhoff M, Wieler LH, Genersch E. 2008. Fluorescence in situ hybridization (FISH) analysis of the interactions between honeybee larvae and Paenibacillus larvae, the causative agent of American foulbrood of honeybees (Apis mellifera). Environ. Microbiol. 10:1612-1620.