Variation in honey bee gut microbial diversity affected by ontogenetic stage, age and geographic location

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Hroncova, Zuzana ^a   Havlik, Jaroslav ^a   Killer, Jiri ^a,b   Doskocil, Ivo ^a   Tyl, Jan ^c   Kamler, Martin ^c   Titera, Dalibor ^a,c   Hakl, Josef ^a   Mrazek, Jakub ^b   Bunesova, Vera ^a   Rada, Vojtech ^a  

^a CZECH UNIVERSITY OF LIFE SCIENCES PRAGUE   (Czech Republic)

^b INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

^c Bee Research Institute at Dol   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; APIS MELLIFERA; ARTICLE; BACTERIAL COUNT; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; DEVELOPMENTAL STAGE; DRONE; FORAGING; GAMMAPROTEOBACTERIA; GEOGRAPHY; GILLIAMELLA APICOLA; INTESTINE; LACTOBACILLUS; LARVA; MICROBIAL DIVERSITY; MICROBIAL POPULATION DYNAMICS; NONHUMAN; POPULATION ABUNDANCE; PUPATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REDUNDANCY ANALYSIS; ANIMAL; BACTERIUM; BEE; CLASSIFICATION; ECOSYSTEM; EMBRYOLOGY; GASTROINTESTINAL TRACT; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTESTINE FLORA; ISOLATION AND PURIFICATION; LACTOBACILLACEAE; MICROBIOLOGY;

APIS MELLIFERA; APOIDEA; BACTERIA (MICROORGANISMS); FIRMICUTES; GAMMAPROTEOBACTERIA;

BACTERIAL DNA; RNA 16S;

ANIMALS; BACTERIA; BEES; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA, BACTERIAL; ECOSYSTEM; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; LACTOBACILLACEAE; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S;

EID: 84929999886     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118707     Document Type: Article

References (46)

1. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, et al. Importance of pollinators in changing landscapes for world crops. ProcBiol Sci. 2007;274:303-313. PMID: 17164193
2. Genersch E. Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol. 2010;87:87-97. doi: 10.1007/s00253-010-2573-8 PMID: 20401479
3. Forsgren E, Olofsson TC, Vásquez A, Fries I. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie. 2010;41:99-108.
4. Evans JD, Lopez DL. Bacterial Probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). J Econ Entomol. 2004;97:752-756. PMID: 15279248
5. Martinson VG, Moy J, Moran NA. Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol. 2012;78:2830-2840. doi: 10.1128/AEM.07810-11 PMID: 22307297
6. Jeyaprakash A, Hoy MA, Allsopp MH. Bacterial diversity in worker adults of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) assessed using 16S rRNA sequences. J Invertebr Pathol. 2003;84:96-103. PMID: 14615218
7. Engel P, Moran NA. Functional and evolutionary insights into the simple yet specific gut microbiota of the honey bee from metagenomic analysis. Gut Microbes. 2013;4:60-65. doi: 10.4161/gmic.22517 PMID: 23060052
8. Mattila HR, Rios D, Walker-Sperling VE, Roeselers G, Newton I L G. Characterization of the active microbiotas associated with honey bees reveals healthier and broader communities when colonies are genetically diverse. PloSOne. 2012;7:e32962. doi: 10.1371/journal.pone.0032962 PMID: 22427917
9. Mrazek J, Strosova L, Fliegerova K, Kott T, Kopecny J. Diversity of insect intestinal microflora. Folia Microbiol (Praha). 2008;53:229-233. doi: 10.1007/s12223-008-0032-z PMID: 18661298
10. Yoshiyama M, Kimura K. Bacteria in the gut of Japanese honeybee, Apis ceranajaponica, and their antagonistic effect against Paenibacillus larvae, the causal agent of American foulbrood. J Invertebr Pathol. 2009;102:91-96. doi: 10.1016/j.jip. 2009.07.005 PMID: 19616552
11. 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;8:258-272. PMID: 16423014
12. Corby-Harris V, Maes P, Anderson KE. The Bacterial Communities Associated with Honey Bee (Apis mellifera) Foragers. PloS One. 2014;9:e95056. doi: 10.1371/journal.pone.0095056 PMID: 24740297
13. Ludvigsen J. Seasonal trends in the midgut microbiota of honeybees. PhD Thesis, Norwegian University of Life Sciences. 2013. Available: http://brage.bibsys.no/xmlui/handle/11250/186492. Accessed 17 June 2014.
14. Gilliam M, Prest DB. Microbiology of feces of the larval honey-bee, Apis-mellifera. J Invertebr Pathol. 1987;49:70-75.
15. Kwong WK, Moran NA. 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 sistertaxon to the order 'Enterobacteriales' of the Gammaproteobacteria. Int J Syst Evol Microbiol. 2013;63:2008-2018. doi: 10.1099/ijs.0.044875-0 PMID: 23041637
16. 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:e36393. doi: 10.1371/journal. pone.0036393 PMID: 22558460
17. Koch H, Abrol DP, Li JL, Schmid-Hempel P. Diversity and evolutionary patterns of bacterial gut associates of corbiculate bees. Mol Ecol. 2013;22:2028-2044. doi: 10.1111/mec.12209 PMID: 23347062
18. Engel P, Stepanauskas R, Moran NA. Hidden diversity in honey bee gut symbionts detected by singlecell genomics. PLoS Genet. 2014;10:e1004596. doi: 10.1371/journal.pgen. 1004596 PMID: 25210772
19. Corby-Harris V, Snyder LA, Schwan MR, Maes P, McFrederick QS, et al. Origin and effect of Acetobacteraceae Alpha 2.2 in honeybee larvae and description of Parasaccharibacterapium, gen. nov., sp. nov. Appl Environ Microbiol. 2014;80:7460-7472. doi: 10.1128/AEM.02043-14 PMID: 25239902
20. Ahn J-H, Hong I-P, Bok J-I, Kim B-Y, Song J, et al. Pyrosequencing analysis of the bacteria communities in the guts of honey bees Apis cerana and Apis mellifera in Korea. Internet J Microbiol. 2012;50:735-745.
21. Olofsson TC, Vasquez A. Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Curr Microbiol. 2008;57:356-363. doi: 10.1007/s00284-008-9202-0 PMID: 18663527
22. Patruica S, Mot D. The effect of using prebiotic and probiotic products on intestinal micro-flora of the honeybee (Apis mellifera carpatica). Bull Entomol Res. 2012;102:619-623. doi: 10.1017/S0007485312000144 PMID: 22459313
23. Olofsson TC, Alsterfjord M, Nilson B, Butler É, Vásquez A. Lactobacillus apinorum sp. nov., Lactobacillus mellifersp. nov., Lactobacillusmellis sp. nov., Lactobacillusmelliventris sp. nov., Lactobacillus kimbladii sp. nov., Lactobacillus helsingborgensis sp. nov., and Lactobacillus kullabergensis sp. nov., isolated from the honey stomach of the honeybee Apis mellifera. Int J Syst Evol Microbiol. 2014;64:3109-3119. doi: 10.1099/ijs.0.059600-0 PMID: 24944337
24. Killer J, Dubna S, Sedlacek I, Svec P. Lactobacillus apis sp. nov., from the stomach of honeybees (Apis mellifera) having in vitro inhibitory effect on causative agents of American and European Foulbrood. Int J Syst Evol Microbiol. 2013;64:152-157. doi: 10.1099/ijs.0.053033-0 PMID: 24096349
25. Killer J, Kopecny J, Mrazek J, Rada V, Benada O, et al. Bifidobacterium bombi sp nov., from the bumblebee digestive tract. Int J Syst Evol Microbiol. 2009;59:2020-2024. doi: 10.1099/ijs.0.002915-0 PMID: 19567560
26. Killer J, Kopecny J, Mrazek J, Havlik J, Koppova I, et al. Bombiscardovia coagulans gen. nov., sp nov., a new member of the family Bifidobacteriaceae isolated from the digestive tract of bumblebees. Syst Appl Microbiol. 2010;33:359-366. doi: 10.1016/j.syapm.2010.08.002 PMID: 20950979
27. Killer J, Kopecny J, Mrazek J, Koppova I, Havlik J, et al. Bifidobacterium actinocoloniiforme sp nov and Bifidobacterium bohemicum sp nov., from the bumblebee digestive tract. Int J Syst Evol Microbiol. 2011;61:1315-1321. doi: 10.1099/ijs.0.022525-0 PMID: 20656822
28. Engel P, Kwong WK, Moran NA. Frischellaperrara gen. nov., sp. nov., a gammaproteobacterium isolated from the gut of the honeybee, Apis mellifera. Int J Syst Evol Microbiol. 2013;63:3646-3651. doi: 10. 1099/ijs.0.049569-0 PMID: 23606484
29. Engel P, Martinson VG, Moran NA. Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci USA. 2012;109:11002-11007. doi: 10.1073/pnas.1202970109 PMID: 22711827
30. Yun Ji-Hyun, et al. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl Environ Microbiol. 2014;80. 17:5254-5264 doi: 10.1128/AEM. 01226-14 PMID: 24928884
31. De F Michelette ER, Soares A E E. Characterization of preimaginal developmental stages in Africanized honey bee workers (Apis mellifera L). Apidologie. 1993;24:431-440.
32. Rembold H, Kremer J-P, Ulrich GM. Characterization of postembryonic developmental stages. Apidologie. 1980;11:29-38.
33. Rettedal EA, Clay S, Brözel VS. GC-clamp primer batches yield 16S rRNA gene amplicon pools with variable GC clamps, affecting denaturing gradient gel electrophoresis profiles. FEMS Microbiol Lett. 2010;312:55-62. doi: 10.1111/j.1574-6968.2010.02097.x PMID: 20831594
34. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol. 2010;28:2731-2739.
35. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540-552. PMID: 10742046
36. De Gregoris TB, Aldred N, Clare AS, Burgess JG. Improvement of phylum- and class-specific primers for real-time PCR quantification of bacterial taxa. J Microbiol Methods. 2011;86:351-356. doi: 10. 1016/j.mimet.2011.06.010 PMID: 21704084
37. Braak C J Ft, Šmilauer P. CANOCO reference manual and CanoDrawfor Windows user's guide: software for canonical community ordination (version 4.5). Section on Permutation Methods Microcomputer Power, Ithaca, New York; 2002.
38. Huang Z-Y, Robinson GE. Regulation of honey bee division of labor by colony age demography. Behav Ecol Sociobiol. 1996;39:147-158.
39. Vasquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, et al. Symbiontsas Major Modulators of Insect Health: Lactic Acid Bacteria and Honeybees. PlosOne. 2012;7:e33188. doi: 10.1371/journal.pone. 0033188 PMID: 22427985
40. Vojvodic S, Rehan SM, Anderson KE. Microbial Gut diversity of Africanized and European honey Bee larval instars. PloSOne. 2013;8:e72106. doi: 10.1371/journal.pone.0072106 PMID: 23991051
41. Gilliam M. Microbial sterility of the intestinal content of the immature honey bee, Apis mellifera. Ann Entomol SocAm. 1971;64:315-316.
42. Kikuchi Y, Hosokawa T, Fukatsu T. Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol. 2007;73:4308-4316. PMID: 17483286
43. Powell JE, Martinson VG, Urban-Mead K, Moran NA. Routes of acquisition of the gut microbiota of Apis mellifera. Appl Environ Microbiol. 2014;80:7378-7387.
44. Ahn J-H, Hong I-P, Bok J-I, Kim B-Y, Song J, et al. Pyrosequencing analysis of the bacterial communities in the guts of honey bees Apis cerana and Apis mellifera in Korea. Internet J Microbiol. 2012;50:735-745.
45. Killer J, Votavova A, Valterova I, Vlkova E, Rada V, et al. Lactobacillus bombi sp. nov., from the digestive tract of laboratory-reared bumblebee queens (Bombus terrestris). Int J Syst Evol Microbiol. 2014;64:2611-2617. doi: 10.1099/ijs.0.063602-0 PMID: 24824637
46. Killer J, Mrázek J, Bunešová V, Havlík J, KoppováI, et al. Pseudoscardoviasuis gen. nov., sp. nov., a new member of the family Bifidobacteriaceae isolated from the digestive tract of wild pigs (Sus scrofa). Syst Appl Microbiol. 2013;36:11-16. doi: 10.1016/j.syapm.2012.09.001 PMID: 23122702