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

Volumn 8, Issue 12, 2013, Pages

  Anderson, Kirk E ^a,b   Sheehan, Timothy H ^a,b   Mott, Brendon M ^b,c   Maes, Patrick ^a,b   Snyder, Lucy ^b   Schwan, Melissa R ^b   Walton, Alexander ^b,d   Jones, Beryl M ^b,e   Corby Harris, Vanessa ^b  

^a UNIVERSITY OF ARIZONA   (United States)

^b CARL HAYDEN BEE RESEARCH CENTER   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

^d IOWA STATE UNIVERSITY   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

DNA 16S;

16S RRNA GENE; ACETOBACTERACEAE; ACTINOBACTERIA; AMPLICON; APIS MELLIFERA; ARTICLE; BACTERIAL GENE; BACTERIAL TRANSMISSION; BACTERIAL VIABILITY; BACTERIUM CULTURE; DIGESTIVE SYSTEM; DNA SEQUENCE; FOOD PRESERVATION; HONEY; LACTOBACILLUS; LACTOBACILLUS KUNKEEI; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MOLECULAR CLONING; NECTAR; NONHUMAN; NUCLEOTIDE SEQUENCE; POLLEN; POLLINATION;

ANIMALS; BACTERIA; BACTERIOLOGICAL TECHNIQUES; BEES; DNA, BACTERIAL; ECOLOGY; ENDOPHYTES; GASTROINTESTINAL TRACT; HONEY; PLANT NECTAR; POLLINATION; RNA, RIBOSOMAL, 16S; SYMBIOSIS;

EID: 84891372560     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083125     Document Type: Article

References (110)

1. Runckel C, Flenniken ML, Engel JC, Ruby JG, Ganem D, et al. (2011) Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS One 6: e20656. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= 3110205&tool=pmcentrez&rendertype=abstract. Accessed 28 February 2013.
2. Cornman RS, Tarpy DR, Chen Y, Jeffreys L, Lopez D, et al. (2012) Pathogen webs in collapsing honey bee colonies. PLoS One 7: e43562. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3424165&tool= pmcentrez&rendertype=abstract. Accessed 8 March 2013.
3. Mullin C a, Frazier M, Frazier JL, Ashcraft S, Simonds R, et al. (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One 5: e9754. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2841636&tool= pmcentrez&rendertype=abstract.
4. Pettis JS, vanEngelsdorp D, Johnson J, Dively G (2012) Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99: 153-158. Available: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=3264871&tool=pmcentrez&rendertype=abstract. Accessed 5 March 2013.
5. 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. Available: http://www. springerlink.com/index/10.1007/s00040-011-0194-6.
6. Gilliam M (1997) Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiol Lett 155: 1-10. Available: http://www3.interscience.wiley.com/journal/119173621/abstract.
7. Martinson VG, Moy J, Moran NA (2012) Establishment of characteristic gut bacteria during development of the honey bee worker. Appl Environ Microbiol 78: 2830-2840. Available: http://www.ncbi.nlm.nih.gov/pubmed/22307297.
8. Moran NA, Hansen AK, Powell JE, Sabree ZL (2012) Distinctive Gut Microbiota of Honey Bees Assessed Using Deep Sampling from Individual Worker Bees. PLoS One 7: e36393. Available: http://dx.plos.org/10.1371/journal.pone. 0036393.
9. Michener CD (1974) The Social Behavior of the Bees: A Comparative Study. Harvard University Press. Available: http://books.google.com/books?hl=en&lr= &id=aordrL-D-30C&pgis=1.
10. Hölldobler B, Wilson EO (2008) The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies. W. W. Norton & Company. Available: http://www.amazon.com/Superorganism-Beauty-Elegance-Strangeness- Societies/dp/0393067041.
11. Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49: 71-92. Available: http://www.ncbi.nlm.nih. gov/pubmed/14651457.
12. Moran N a, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42: 165-190. Available: http://www.ncbi.nlm.nih.gov/pubmed/18983256.
13. Feldhaar H, Gross R (2009) Genome degeneration affects both extracellular and intracellular bacterial endosymbionts. J Biol 8: 31. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2689433&tool= pmcentrez&rendertype=abstract.
14. Gibson CM, Hunter MS (2010) Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecol Lett 13: 223-234. Available: http://www.ncbi.nlm.nih.gov/pubmed/ 20015249.
15. Russell J a, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, et al. (2009) Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci U S A 106: 21236-21241. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2785723&tool= pmcentrez&rendertype=abstract.
16. Anderson KE, Russell J a, Moreau CS, Kautz S, Sullam KE, et al. (2012) Highly similar microbial communities are shared among related and trophically similar ant species. Mol Ecol 21: 2282-2296. Available: http://www.ncbi.nlm.nih. gov/pubmed/22276952.
17. Troyer K (1984) Behavioral acquisition of the hindgut fermentation system by hatchling Iguana iguana. Behav Ecol Sociobiol 14: 189-193. Available: http://www.springerlink.com/index/10.1007/BF00299618.
18. Ohkuma M (2001) Symbiosis within the gut microbial community of termites. RIKEN Rev 41: 69-72.
19. Engel P, Martinson VG, Moran NA (2012) Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci U S A 109: 1-6. Available: http://www.ncbi.nlm.nih.gov/pubmed/22711827.
20. Gordon DM (2001) Geographical structure and host specificity in bacteria and the implications for tracing the source of coliform contamination. Microbiology 147: 1079-1085. Available: http://www.ncbi.nlm.nih.gov/pubmed/ 11320111.
21. Kikuchi Y, Hosokawa T, Nikoh N, Meng X-Y, Kamagata Y, et al. (2009) Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biol 7: 2. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2637841&tool= pmcentrez&rendertype=abstract.
22. Crotti E, Rizzi A, Chouaia B, Ricci I, Favia G, et al. (2010) Acetic acid bacteria, newly emerging symbionts of insects. Appl Environ Microbiol 76: 6963-6970. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= 2976266&tool=pmcentrez&rendertype=abstract. Accessed 6 March 2013.
23. 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. Available: http://www.ncbi.nlm.nih.gov/pubmed/16423014.
24. 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. Available: http://www.ncbi.nlm.nih.gov/pubmed/17381517.
25. 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. Available: http://www.ncbi.nlm.nih.gov/pubmed/17823314.
26. 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. Available: http://www.ncbi.nlm.nih.gov/pubmed/ 21175905.
27. Sabree ZL, Hansen AK, Moran NA (2012) Independent Studies Using Deep Sequencing Resolve the Same Set of Core Bacterial Species Dominating Gut Communities of Honey Bees. PLoS One 7: e41250. Available: http://dx.plos.org/10. 1371/journal.pone.0041250.
28. Crailsheim K (1988) Regulation of food passage in the intestine of the honeybee (Apis mellifera L.). J Insect Physiol 34: 85-90. Available: http://dx.doi.org/10.1016/0022-1910(88)90158-8.
29. Olofsson TC, Vásquez 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. Available: http://www.ncbi.nlm.nih.gov/ pubmed/18663527.
30. 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. Available: http://www.ibra.org.uk/articles/20090701-9.
31. Olofsson TC, Vásquez A (2009) Phylogenetic comparison of bacteria isolated from the honey stomachs of honey bees Apis mellifera andbumble bees Bombus spp. J Apic Res 48: 233-237. Available: http://www.ibra.org.uk/articles/ 20090911-2.
32. Vásquez A, Olofsson TC (2011) The honey crop - the holy Grail when antibiotics fail. Microbiol Today 38: 226-229.
33. Vásquez 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. Available: http://dx.plos.org/10.1371/journal. pone.0033188.
34. Hall TA (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
35. Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319. Available: http://www.ncbi.nlm.nih.gov/pubmed/15073015.
36. DeSantis TZ, Hugenholtz P, Larsen N (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench. Appl Environ Microbiol. Available: http://aem.asm.org/cgi/content/abstract/72/7/5069.
37. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, et al. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145. Available: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=2686447&tool=pmcentrez&rendertype=abstract.
38. Kwong WK, Moran N a (2012) 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. Int J Syst Evol Microbiol. Available: http://www.ncbi.nlm.nih.gov/pubmed/23041637. Accessed 9 October 2012.
39. Gotelli NJ (2002) EcoSim: null models software for ecology. Version 7.0. Jericho VT, USA.
40. Mattila HR, Rios D, Walker-Sperling VE, Roeselers G, Newton ILG (2012) Characterization of the Active Microbiotas Associated with Honey Bees Reveals Healthier and Broader Communities when Colonies are Genetically Diverse. PLoS One 7: e32962. Available: http://dx.plos.org/10.1371/journal.pone.0032962.
41. Newton IL, 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. Available: http://www.ncbi.nlm.nih.gov/pubmed/23013113. Accessed 5 October 2012.
42. 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 Biotechnol 75: 573-582. Available: http://www.ncbi.nlm.nih.gov/pubmed/17273854. Accessed 27 February 2013.
43. Chen YP, Huang ZY (2010) Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie 41: 364-374. Available: http://www.apidologie.org/10.1051/apido/2010021.
44. Disayathanoowat T, Young JPW, Helgason T, Chantawannakul P (2012) TRFLP analysis of bacterial communities in the midguts of Apis mellifera and Apis cerana honey bees in Thailand. FEMS Microbiol Ecol 79: 273-281. Available: http://www.ncbi.nlm.nih.gov/pubmed/22092273. Accessed 15 March 2013.
45. Hendriksma HP, Küting M, Härtel S, Näther A, Dohrmann AB, et al. (2013) Effect of Stacked Insecticidal Cry Proteins from Maize Pollen on Nurse Bees (Apis mellifera carnica) and Their Gut Bacteria. PLoS One 8: e59589. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= 3606186&tool=pmcentrez&rendertype=abstract. Accessed 2 April 2013.
46. Evans J, Sheneman L, Foster J (2006) Relaxed neighbor joining: a fast distance-based phylogenetic tree construction method. J Mol Evol 62: 785-792. Available: http://www.ncbi.nlm.nih.gov/pubmed/16752216.
47. Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4: 17-27. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2797552&tool= pmcentrez&rendertype=abstract.
48. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, et al. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196. Available: http://www.ncbi.nlm.nih.gov/pubmed/17947321.
49. Schloss PD (2009) A High-Throughput DNA Sequence Aligner for Microbial Ecology Studies. PLoS One 4: 9. Available: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=2788221&tool=pmcentrez&rendertype=abstract.
50. 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. Available: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=1950982&tool=pmcentrez&rendertype=abstract.
51. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452. Available: http://www.ncbi.nlm.nih.gov/pubmed/19346325. Accessed 6 August 2013.
52. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599. Available: http://www.ncbi.nlm.nih.gov/pubmed/17488738. Accessed 28 February 2013.
53. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425. Available: http://www.ncbi.nlm.nih.gov/pubmed/18343690.
54. Felsenstein J (1985) Confidence limits on phylogenies:An approach using the bootstrap. Evolution (N Y) 39: 783-791.
55. Engel (2013) Frischella perrara gen. nov., sp. nov., a gammaproteobacterium isolated from the gut of the honey bee, Apis mellifera. Int J Syst Evol Microbiol doi:10.109.
56. Martin D, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. 16: 562-563.
57. Dawkins R (2004) Extended Phenotype - But Not Too Extended. A Reply to Laland, Turner and Jablonka: 377-396.
58. McFrederick QS, Cannone JJ, Gutell RR, Kellner K, Plowes RM, et al. (2013) Specificity between Lactobacilli and Hymenopteran Hosts Is the Exception Rather than the Rule. Appl Environ Microbiol 79: 1803-1812. Available: http://www.ncbi.nlm.nih.gov/pubmed/23291551. Accessed 13 March 2013.
59. Turner JS (2005) Extended Physiology of an Insect-Built Structure: 36-38.
60. Judd TM (2011) The role of food storage and communication in the evolution of perennial social Hymenopteran colonies. In: Stewart EM, Social insects: Structure, Function and Behavior. Nova.
61. Rosengaus RB, Moustakas JE, Calleri DV, Traniello JF a (2003) Nesting ecology and cuticular microbial loads in dampwood (Zootermopsis angusticollis) and drywood termites (Incisitermes minor, I. schwarzi, Cryptotermes cavifrons). J Insect Sci 3: 31. Available: http://www.pubmedcentral.nih.gov/articlerender. fcgi?artid=524670&tool=pmcentrez&rendertype=abstract.
62. Turner JS (2004) Extended Phenotypes and Extended Organisms: 327-352.
63. Hughes DP, Pierce NE, Boomsma JJ (2008) Social insect symbionts: evolution in homeostatic fortresses. Trends Ecol Evol 23: 672-677. Available: http://www.ncbi.nlm.nih.gov/pubmed/18951653. Accessed 11 March 2013.
64. 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 Biotechnol 75: 573-582. Available: http://www.ncbi.nlm.nih.gov/pubmed/17273854. Accessed 27 February 2013.
65. Jeyaprakash A, Hoy M a., 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. Available: http://linkinghub.elsevier.com/retrieve/pii/S0022201103001411.
66. Ahn J-H, Hong I-P, Bok J-I, Kim B-Y, Song J, et al. (2012) Pyrosequencing analysis of the bacterial communities in the guts of honey bees Apis cerana and Apis mellifera in Korea. J Microbiol 50: 735-745. Available: http://www.ncbi.nlm.nih.gov/pubmed/23124740. Accessed 16 April 2013.
67. Rangberg A, Diep DB, Rudi K, Amdam G V (2012) Paratransgenesis: An Approach to Improve Colony Health and Molecular Insight in Honey Bees (Apis mellifera)? Integr Comp Biol 52: 1-11. Available: http://www.ncbi.nlm.nih.gov/ pubmed/22659204.
68. Neveling DP, Endo A, Dicks LMT (2012) Fructophilic Lactobacillus kunkeei and Lactobacillus brevis Isolated from Fresh Flowers, Bees and Bee-hives. Curr Microbiol. Available: http://www.ncbi.nlm.nih.gov/pubmed/22797888.
69. Koch H, Schmid-Hempel P (2011) Bacterial communities in central European bumblebees: low diversity and high specificity. Microb Ecol 62: 121-133. Available: http://www.ncbi.nlm.nih.gov/pubmed/21556885.
70. Endo A, Futagawa-Endo Y, Dicks LMT (2009) Isolation and characterization of fructophilic lactic acid bacteria from fructose-rich niches. Syst Appl Microbiol 32: 593-600. Available: http://www.ncbi.nlm.nih.gov/pubmed/19733991.
71. Endo A, Irisawa T, Futagawa-Endo Y, Takano K, Du Toit M, et al. (2011) Characterization and emended description of Lactobacillus kunkeei as a fructophilic lactic acid bacterium. Int J Syst Evol Microbiol. Available: http://www.ncbi.nlm.nih.gov/pubmed/21478398.
72. 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. Available: http://www.ncbi.nlm.nih.gov/pubmed/22340254.
73. Ruiz-Argueso T, Rodriguez-Navarro a (1975) Microbiology of ripening honey. Appl Microbiol 30: 893-896. Available: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=376564&tool=pmcentrez&rendertype=abstract.
74. Disayathanoowat T, Young JPW, Helgason T, Chantawannakul P (2011) T-RFLP analysis of bacterial communities in the midguts of Apis mellifera and Apis cerana honey bees in Thailand. Fems Micriobiology Ecol 79: 273-281. Available: http://doi.wiley.com/10.1111/j.1574-6941.2011.01216.x.
75. García AH (2011) Anhydrobiosis in bacteria: from physiology to applications. J Biosci 36: 939-950. Available: http://www.ncbi.nlm.nih.gov/ pubmed/22116292.
76. Millet V, Lonvaud-Funel A (2000) The viable but non-culturable state of wine micro-organisms during storage. Lett Appl Microbiol 30: 136-141. Available: http://www.ncbi.nlm.nih.gov/pubmed/10736016.
77. Ruiz-Argüeso T, Rodriguez-Navarro A (1973) Gluconic acid-producing bacteria from honey bees and ripening honey. J Gen Microbiol 76: 211-216. Available: http://www.ncbi.nlm.nih.gov/pubmed/4579122.
78. Shamala TR, Shri Jyothi Y, Saibaba P (2000) Stimulatory effect of honey on multiplication of lactic acid bacteria under in vitro and in vivo conditions. Lett Appl Microbiol 30: 453-455. Available: http://www.blackwell-synergy.com/ doi/abs/10.1046/j.1472-765x.2000.00746.x.
79. Aween MM, Hassan Z, Muhialdin BJ, Eljamel Y a, Al-Mabrok ASW, et al. (2012) Antibacterial activity of Lactobacillus acidophilus strains isolated from honey marketed in Malaysia against selected multiple antibiotic resistant (MAR) Gram-positive bacteria. J Food Sci 77: M364-71. Available: http://www.ncbi.nlm. nih.gov/pubmed/22757710. Accessed 3 October 2012.
80. Gupta AK, Nayduch D, Verma P, Shah B, Ghate H V, et al. (2012) Phylogenetic characterization of bacteria in the gut of house flies (Musca domestica L.). FEMS Microbiol Ecol 79: 581-593.Available: http://www.ncbi.nlm. nih.gov/pubmed/22092755. Accessed 25 March 2013.
81. Kautz S, Rubin BER, Russell J a, Moreau CS (2013) Surveying the microbiome of ants: comparing 454 pyrosequencing with traditional methods to uncover bacterial diversity. Appl Environ Microbiol 79: 525-534. Available: http://www.ncbi.nlm.nih.gov/pubmed/23124239. Accessed 28 February 2013.
82. Vojvodic S, Rehan SM, Anderson KE (2013) Microbial Gut Diversity of Africanized and European Honey Bee Larval Instars. PLoS One 8: e72106. Available: http://dx.plos.org/10.1371/journal.pone.0072106. Accessed 26 August 2013.
83. Bution ML, Caetano FH (2008) Ileum of the Cephalotes ants: a specialized structure to harbor symbionts microorganisms. Micron Oxford Engl 1993 39: 897-909. Available: http://www.ncbi.nlm.nih.gov/pubmed/18187330.
84. Brucker RM, Bordenstein SR (2012) The roles of host evolutionary relationships (genus: Nasonia) and development in structuring microbial communities. Evolution 66: 349-362. Available: http://www.ncbi.nlm.nih.gov/ pubmed/22276533. Accessed 13 August 2013.
85. Kacániová M, Chlebo R, Kopernický M, Trakovická a (2004) Microflora of the honeybee gastrointestinal tract. Folia Microbiol (Praha) 49: 169-171. Available: http://www.ncbi.nlm.nih.gov/ pubmed/22937713.
86. Rada V, Máchová M, Huk J, Marounek M, Dušková D (1997) Microflora in the honeybee digestive tract: counts, characteristics and sensitivity to veterinary drugs. Apidologie 28: 357-365. Available: http://www.apidologie.org/10.1051/apido:19970603.
87. Loper GM, Standifer LN, Thompson MJ, Gilliam M (1980) Biochemistry and microbiology of bee-collected almond (Prunus dulcis) pollen and beebread. I-Fatty Acids, Sterols, Vitamins and Minerals. Apidologie 11: 63-73. Available: http://www.cabdirect.org/abstracts/19800210999.html?freeview=true.
88. Daeschel MA, Andersson RE, Fleming HP (1987) Microbial ecology of fermenting plant materials. FEMS Microbiol Lett 46: 357-367. Available: http://www.sciencedirect.com/science/article/pii/0378109787901194.
89. 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. Available: http://www.ncbi.nlm.nih.gov/pubmed/15545468.
90. Gilliam M, Lorenz BJ (1983) Gram-positive cocci from apiarian sources. J Invertebr Pathol 42: 187-195. Available: http://dx.doi.org/10.1016/0022-2011(83) 90061-7.
91. Inglis GD, Sigler L, Goette MS (1993) Aerobic microorganisms associated with alfalfa leafcutter bees (megachile rotundata). Microb Ecol 26: 125-143. Available: http://link.springer.com/article/10.1007/BF00177048.
92. Promnuan Y, Kudo T, Chantawannakul P (2009) Actinomycetes isolated from beehives in Thailand. World J Microbiol Biotechnol 25: 1685-1689. Available: http://www.springerlink.com/index/10.1007/s11274-009-0051-1.
93. Vidaver AK (1982) The plant pathogenic corynebacteria. Annu Rev Microbiol 36: 495-517. Available: http://www.annualreviews.org/doi/abs/10.1146/annurev. mi.36.100182.002431.
94. Currie CR, Scott JA (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398: 701-705. Available: http:// cas.bellarmine.edu/tietjen/Ecology/fungus.htm.
95. Kaltenpoth M (2009) Actinobacteria as mutualists: general healthcare for insects? Trends Microbiol 17: 529-535. Available: http://www.ncbi.nlm.nih.gov/ pubmed/19853457.
96. Barke J, Seipke RF, Grüschow S, Heavens D, Drou N, et al. (2010) A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus. BMC Biol 8: 109. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2942817&tool= pmcentrez&rendertype=abstract.
97. Seipke RF, Barke J, Brearley C, Hill L, Yu DW, et al. (2011) A Single Streptomyces Symbiont Makes Multiple Antifungals to Support the Fungus Farming Ant Acromyrmex octospinosus. PLoS One 6: 8. Available: http://dx.plos.org/10. 1371/journal.pone.0022028.
98. Gilliam M, Prest DB (1987) Microbiology of feces of the larval honey bee, Apis mellifera. J Invertebr Pathol 49: 70-75. Available: http://www. researchgate.net/publication/223680621-Microbiology-of-feces-of-the-larval- honey-bee-Apis-mellifera.
99. Koch H, Abrol DP, Li J, Schmid-Hempel P (2013) Diversity and evolutionary patterns of bacterial gut associates of corbiculate bees. Mol Ecol: 2028-2044.Available: http://www.ncbi.nlm.nih.gov/pubmed/23347062. Accessed 11 March 2013.
100. Bottacini F, Milani C, Turroni F, Sánchez B, Foroni E, et al. (2012) Bifidobacterium asteroides PRL2011 Genome Analysis Reveals Clues for Colonization of the Insect Gut. PLoS One 7: e44229.Available: http://www.ncbi.nlm.nih.gov/pubmed/23028506. Accessed 3 October 2012.
101. Fridman S, Izhaki I, Gerchman Y, Halpern M (2012) Bacterial communities in floral nectar. Environ Microbiol Rep 4: 97-104. Available: http://doi.wiley.com/10.1111/j.1758-2229.2011.00309.x. Accessed 15 March 2013.
102. Alvarez-Pérez S, Herrera CM, de Vega C (2012) Zooming-in on floral nectar: a first exploration of nectar-associated bacteria in wild plant communities. FEMS Microbiol Ecol 80: 591-602. Available: http://www.ncbi.nlm. nih.gov/pubmed/22324904. Accessed 15 March 2013.
103. Suzuki I, Nomura M, Morichi T (1991) Isolation of lactic acid bacteria which suppress mold growth and show antifungal action. Milchwissenschaft 46: 635-639.
104. Forsgren E, Olofsson TC, Vásquez A, Fries I (2009) Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41: 99-108. Available: http://www.apidologie.org/10.1051/apido/2009065.
105. Pain J, Maugenet J. (1966) Recherches biochimiques et physiologiques sur le pollen emmagsiné par les abeilles. Ann Abeille 9: 209-236. Available: http://honeybee.drawwing.org/node/573.
106. Microbiome F, Shade A, Mcmanus PS, Handelsman J (2013) Unexpected Diversity during Community Succession in the Apple Flower Microbiome. doi:10.1128/mBio.00602-12.Editor.
107. McFrederick QS, Cannone JJ, Gutell RR, Kellner K, Plowes RM, et al. (2013) Specificity between Lactobacilli and Hymenopteran Hosts Is the Exception Rather than the Rule. Appl Environ Microbiol 79: 1803-1812. Available: http://www.ncbi.nlm.nih.gov/pubmed/23291551. Accessed 13 March 2013.
108. Piccini C., Antunez K., Zunino P. (2004) An approach to the characterization of the honey bee hive bacterial flora. J Apic Res 43: 101-104. Available: http://openagricola.nal.usda.gov/Record/IND43663050.
109. Evans JD, Armstrong T-N (2006) Antagonistic interactions between honey bee bacterial symbionts and implications for disease. BMC Ecol 6: 4. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1471774&tool= pmcentrez&rendertype=abstract.
110. Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SSK, et al. (2011) Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 108 Suppl: 4680-4687. Available: http://www.pnas.org/cgi/content/abstract/108/Supplement-1/ 4680.