Microbial Gut Diversity of Africanized and European Honey Bee Larval Instars

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Vojvodic, Svjetlana ^a   Rehan, Sandra M ^b   Anderson, Kirk E ^a,c  

^a The University of Arizona   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c United States Department of Agriculture ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL VECTOR; RIBOSOME DNA; ROYAL JELLY;

ACETOBACTERACEAE; AFRICA; ANTIMICROBIAL ACTIVITY; ARTICLE; BACILLUS; BACTERIAL COLONIZATION; BACTERIUM INHIBITION; BACTERIUM ISOLATE; BIFIDOBACTERIUM; COMMUNITY SUCCESSION; CONTROLLED STUDY; DNA SEQUENCE; EUROPE; HONEYBEE; INOCULATION; INTESTINE FLORA; LACTOBACILLUS; LARVAL DEVELOPMENT; LARVAL STAGE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIOLOGICAL PHENOMENA AND FUNCTIONS; NEISSERIACEAE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLLINATOR; SEQUENCE ANALYSIS; STAPHYLOCOCCUS; STREPTOMYCES;

ACETOBACTERACEAE; AFRICA; ANIMALS; BACTERIA; BEES; BIODIVERSITY; DNA BARCODING, TAXONOMIC; DNA, BACTERIAL; EUROPE; GASTROINTESTINAL TRACT; GENETIC VARIATION; LACTOBACILLUS; LARVA; MICROBIOTA; MOLECULAR SEQUENCE DATA; NEISSERIACEAE; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

EID: 84882705545     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072106     Document Type: Article

References (66)

1. Moran NA, (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci USA 104: 8627-8633.
2. Lundgren JG, Lehman RM, (2010) Bacterial gut symbionts contribute to seed digestion in an omnivorous beetle. PLoS ONE 5(5): e10831 doi:10.1371/journal.pone.0010831.
3. Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE, (2009) Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci USA 106: 21236-21241.
4. Janson EM, Stireman III JO, Singer MS, Abbot P, (2008) Phytophagous insectmicrobe mutualisms and adaptive evolutionary diversification. Evolution 62: 997-1012.
5. McCreadie JW, Beard CE, Adler PH, (2005) Context dependent symbiosis between black flies (Diptera: Simuliidae) and trichomycete fungi (Harpellales: Legeriomycetaceae). Oikos 108: 362-370.
6. Ryu J-H, Kim SH, Lee HY, Bai JY, Nam YD, et al. (2008) Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila. Science 319: 777-782.
7. Chouaia B, Rossi P, Epis S, Mosca M, Ricci I, et al. (2012) Delayed larval development in Anopheles mosquitoes deprived of Asaia bacterial symbionts. BMC Microbiol 12(Suppl 1): S2.
8. Shin SC, Sung-Hee K, Hyejin Y, Boram K, Aeri CK, et al. (2011) Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334: 670-674.
9. Storelli G, Defaye A, Erkosar B, Hols P, Royet J, et al. (2011) Lactobacillus plantarum Promotes Drosophila Systemic Growth by Modulating Hormonal Signals through TOR-Dependent Nutrient Sensing. Cell Metabolism 14: 403-414.
10. Pain J, Maugenet J, (1966) Recherches biochimiques et physiologiques sur le pollen emmagasine par les abeilles. Ann Abeille 9: 209-236.
11. Forsgren E, Olofsson TC, Vásquez A, Fries I, (2010) Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41: 99-108.
12. McFrederick Q, 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.
13. 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 4: e36393 doi:10.1371/journal.pone.00363932012.
14. 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 (doi:10.1128/AEM.07810-11).
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).
16. 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.
17. 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.
18. Gilliam M, (1971) Microbial sterility of the intestinal content of the immature honey bee Apis mellifera. Ann Entomol Sac Am 4: 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. Evans JD, Armstrong TA, (2006) Antagonistic interactions between honey bee bacterial symbionts and implications for disease. BMC Ecol 6: 4.
21. Gilliam M, (1997) Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiol Lett 155: 1-10.
22. Gilliam M, (1979a) Microbiology of pollen and bee bread: the yeasts. Apidologie 10: 43-53.
23. Gilliam M, (1979b) Microbiology of pollen and bee bread: the genus Bacillus. Apidologie 10: 269-274.
24. Gilliam M, Lorenz BJ, Richardson GV (1988) Digestive enzymes and micro-organisms in honey bees, Apis mellifera: influence of streptomycin, age, season and pollen. Microbios, 55, 95-114.
25. Beetsma J (1985) Feeding behaviour of nurse bees, larval food composition and caste differentiation in the honeybee (Apis mellifera L). In: Experimental Behavioral Ecology and Sociobiology, Holldobler B, Lindauer M, editors. Sinauer Associates: Sunderland, UK. 407-410.
26. Bilikova K, Hanes J, Nordhoff E, Saenger W, Klaudiny J, et al. (2002) Apisimin, a new serine-valine-rich peptide from honeybee (Apis mellifera L.) royal jelly: purification and molecular characterization. FEBS Lett 528: 125-129.
27. Fontana R, Mendes MA, de Souza BM, Konno K, Cesar LMM, et al. (2004) Jelleines: a family of antimicrobial peptides from the royal jelly of honeybees (Apis mellifera). Peptides 25: 919-928.
28. Winston ML (1991) The Biology of the Honeybee. Harvard University Press: Cambridge Mass USA.
29. Bailey L, Ball BV (1991) Honeybee pathology, 2nd Ed, Academic Press: San Diego USA.
30. Seeley TD (1995) The Wisdom of the Hive, Harvard University Press: Cambridge USA.
31. Gilliam M, Vandenberg JD (1997) Fungi. In Honey bee pests, predators and diseases, 3rd edition. Morse RA, Flottum K, editors. AI Root Co, Medina USA 79-112.
32. Vojvodic S, Jensen AB, James RR, Boomsma JJ, Eilenberg J, (2010) Opposing temperature-dependent mortality after infection with an obligate and facultative fungal pathogen of honeybees. Vet Microbiol 149: 200-205.
33. Rauch S, Ashiralieva A, Hedtke K, Genersch E, (2009) Negative correlation between individual-insect-level virulence and colony-level virulence of Paenibacillus larvae, the etiological agent of American foulbrood of honeybees. Appl Environ Microbiol 75: 3344-3347.
34. Giovannoni SJ (1991) The polymerase chain reaction. In: Nucleic acid techniques in bacterial systematics. Stackebrandt E, Goodfellow M, editors. Wiley New York NY. 177-201.
35. Hall TA, (1999) Bioedit: a user friendly biological sequence alignment editor and alignment program for Windows 95/98 NT. Nucleic Acid Symposium Series 41: 95-98.
36. Katoh M, Kuma M, (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066.
37. Thompson JD, Higgins DG, Gibons TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
38. Swofford DL (2005) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version b4.10. Sinauer Associates Sunderland Massachusetts USA.
39. 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.
40. Neveling DP, Endo A, Dicks LM, (2012) Fructophilic Lactobacillus kunkeei and Lactobacillus brevis isolated from fresh flowers, bees and bee-hives. Curr Microbiol 65: 507-515.
41. Vásquez A, Olofsson TC, Sammataro DA, (2009) Scientific note on the lactic acid bacterial flora in honeybees in the USA - A comparison with bees from Sweden. Apidologie 40: 26-28.
42. Olofsson TC, Vásquez A, Sammataro D, Macharia J (2011) A scientific note on the lactic acid bacterial flora within the honeybee subspecies; Apis mellifera (Buckfast), A. m. scutellata, A. m. mellifera, and A. m. monticola. Apidologie 1-4.
43. Koeppel A, Perry EB, Sikorski J, Krizanc D, Warner A, et al. (2008) Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proc Natl Acad Sci USA 105: 2504-2509.
44. Ramadan MF, Al-Ghamdi A, (2012) Bioactive compounds and health-promoting properties of royal jelly: A review. J Funct Food 4: 39-52.
45. Romanelli A, Moggio L, Montella RC, Campiglia P, Iannaccone M, et al. (2011) Peptides from royal jelly: studies on the antimicrobial activity of jelleins, jelleins analogs and synergy with temporins. J Pept Sci 17: 348-352.
46. Liu JR, Yang YC, Shi LS, Peng CC, (2008) Antioxidant properties of royal jelly associated with larval age and time of harvest. J Agricul Food Chem 56: 11447-11452.
47. García MC, Finola MS, Marioliet JM, (2010) Antibacterial activity of Royal Jelly against bacteria capable of infecting cutaneous wounds. Journal of ApiProduct and ApiMedical Science 2: 93-99.
48. Pavel CI, Mǎrghitaş LA, Bobiş O, Dezmirean DS, Şapcaliu A, et al. (2011) Biological Activities of Royal Jelly - Review. Animal Science and Biotechnologies. 44: 108-118.
49. 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 Sociaux 58: 431-444.
50. Rodriguez-Navarro T, Ruiz-Argueso A, (1973) Gluconic acid producing bacteria from honey bee and ripening honey. J Gen Microbiol 76: 211-216.
51. Rodriguez-Navarro T, Ruiz-Argueso A, (1975) Microbiology of ripening honey. Appl Microbiol 30: 893-896.
52. 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: 453-5.
53. Endo A, Futagawa-Endo Y, Dicks LM, (2009) Isolation and characterization of fructophilic lactic acid bacteria from fructose-rich niches. Syst Appl Microbiol 32: 593-600.
54. Endo A, Irisawa T, Futagawa-Endo Y, Takao E, du Toit M, et al. (2011) Characterization and emended description of Lactobacillus kunkeei as a fructophilic lactic acid bacterium. Int J Syst Evol Microbiol 62: 500-5004.
55. Aween MM, Hassan Z, Muhialdin BJ, Noor MH, Eljamel YA, (2012) Evaluating on antibacterial activity of Lactobacillus acidophilus strains isolated from honey. Am J Applied Sci 9: 807-817.
56. 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.
57. 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.
58. 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.
59. Koch H, Schmid-Hempel P, (2011) Bacterial communities in central European bumblebees: low diversity and high specificity. Microb Ecol 62: 121-133.
60. Disayathanoowat T, Young JPW, Helgason T, Chantawannakul P, (2012) T-RFLP analysis of bacterial communities in the midguts of Apis mellifera and Apis cerana honey bees in Thailand. FEMS Microbiol Ecol 79: 273-281.
61. 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.
62. 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.
63. Dillon RJ, Dillon VM, (2004) The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49: 71-92.
64. Crotti E, Damiani C, Pajoro M, Gonella E, Rizzi A, et al. (2009) Asaia, a versatile acetic acid bacterial symbiont, capable of cross-colonizing insects of phylogenetically distant genera and orders. Environ. Microbiol 11: 3252-3264.
65. Simpson J, (1955) The significance of the presence of pollen in the food of worker larvae of the honey-bee. QJ Microsc Sci 96: 117-120.
66. Batra LR, Batra SWT, Bohart EO, (1973) The mycoflora of domesticated and wild bees (Apoidea). Mycopathologia 49: 13-44.