Microbial Gut Diversity of Africanized and European Honey Bee Larval Instars

The first step in understanding gut microbial ecology is determining the presence and potential niche breadth of associated microbes. While the core gut bacteria of adult honey bees is becoming increasingly apparent, there is very little and inconsistent information concerning symbiotic bacterial co...

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Published inPloS one Vol. 8; no. 8; p. e72106
Main Authors Vojvodic, Svjetlana, Rehan, Sandra M, Anderson, Kirk E, Smagghe, Guy
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 21.08.2013
Public Library of Science (PLoS)
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Abstract The first step in understanding gut microbial ecology is determining the presence and potential niche breadth of associated microbes. While the core gut bacteria of adult honey bees is becoming increasingly apparent, there is very little and inconsistent information concerning symbiotic bacterial communities in honey bee larvae. The larval gut is the target of highly pathogenic bacteria and fungi, highlighting the need to understand interactions between typical larval gut flora, nutrition and disease progression. Here we show that the larval gut is colonized by a handful of bacterial groups previously described from guts of adult honey bees or other pollinators. First and second larval instars contained almost exclusively Alpha 2.2, a core Acetobacteraceae, while later instars were dominated by one of two very different Lactobacillus spp., depending on the sampled site. Royal jelly inhibition assays revealed that of seven bacteria occurring in larvae, only one Neisseriaceae and one Lactobacillus sp. were inhibited. We found both core and environmentally vectored bacteria with putatively beneficial functions. Our results suggest that early inoculation by Acetobacteraceae may be important for microbial succession in larvae. This assay is a starting point for more sophisticated in vitro models of nutrition and disease resistance in honey bee larvae.
AbstractList The first step in understanding gut microbial ecology is determining the presence and potential niche breadth of associated microbes. While the core gut bacteria of adult honey bees is becoming increasingly apparent, there is very little and inconsistent information concerning symbiotic bacterial communities in honey bee larvae. The larval gut is the target of highly pathogenic bacteria and fungi, highlighting the need to understand interactions between typical larval gut flora, nutrition and disease progression. Here we show that the larval gut is colonized by a handful of bacterial groups previously described from guts of adult honey bees or other pollinators. First and second larval instars contained almost exclusively Alpha 2.2, a core Acetobacteraceae, while later instars were dominated by one of two very different Lactobacillus spp., depending on the sampled site. Royal jelly inhibition assays revealed that of seven bacteria occurring in larvae, only one Neisseriaceae and one Lactobacillus sp. were inhibited. We found both core and environmentally vectored bacteria with putatively beneficial functions. Our results suggest that early inoculation by Acetobacteraceae may be important for microbial succession in larvae. This assay is a starting point for more sophisticated in vitro models of nutrition and disease resistance in honey bee larvae.
The first step in understanding gut microbial ecology is determining the presence and potential niche breadth of associated microbes. While the core gut bacteria of adult honey bees is becoming increasingly apparent, there is very little and inconsistent information concerning symbiotic bacterial communities in honey bee larvae. The larval gut is the target of highly pathogenic bacteria and fungi, highlighting the need to understand interactions between typical larval gut flora, nutrition and disease progression. Here we show that the larval gut is colonized by a handful of bacterial groups previously described from guts of adult honey bees or other pollinators. First and second larval instars contained almost exclusively Alpha 2.2, a core Acetobacteraceae, while later instars were dominated by one of two very different Lactobacillus spp., depending on the sampled site. Royal jelly inhibition assays revealed that of seven bacteria occurring in larvae, only one Neisseriaceae and one Lactobacillus sp. were inhibited. We found both core and environmentally vectored bacteria with putatively beneficial functions. Our results suggest that early inoculation by Acetobacteraceae may be important for microbial succession in larvae. This assay is a starting point for more sophisticated in vitro models of nutrition and disease resistance in honey bee larvae.
Audience Academic
Author Rehan, Sandra M
Smagghe, Guy
Anderson, Kirk E
Vojvodic, Svjetlana
AuthorAffiliation 2 Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America
3 United States Department of Agriculture, Tucson, Arizona, United States of America
Ghent University, Belgium
1 Center for Insect Science, Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, United States of America
AuthorAffiliation_xml – name: Ghent University, Belgium
– name: 1 Center for Insect Science, Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona, United States of America
– name: 3 United States Department of Agriculture, Tucson, Arizona, United States of America
– name: 2 Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America
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Cites_doi 10.1093/aesa/64.1.315
10.1002/psc.1316
10.1073/pnas.0907926106
10.1051/apido:19790304
10.4159/9780674043404
10.1128/AEM.02839-08
10.1126/science.1149357
10.1111/j.1558-5646.2008.00348.x
10.1111/j.1365-294X.2010.04959.x
10.1016/S0014-5793(02)03272-6
10.1073/pnas.0712205105
10.1371/journal.pone.0041250
10.1128/AEM.07810-11
10.1093/nar/22.22.4673
10.1051/apido:19660302
10.1016/j.cmet.2011.07.012
10.1371/journal.pone.0036393
10.1186/1472-6785-6-4
10.1111/j.1462-2920.2005.00893.x
10.1016/j.jff.2011.12.007
10.1371/journal.pone.0010831
10.1051/apido:19790106
10.1016/S0378-1097(97)00337-6
10.1093/nar/gkf436
10.1021/jf802494e
10.1099/ijs.0.031054-0
10.1051/apido:2008063
10.1146/annurev.ento.49.061802.123416
10.1111/j.0030-1299.2005.13417.x
10.3896/IBRA.4.02.3.02
10.1046/j.1472-765x.2000.00746.x
10.1007/s00284-008-9202-0
10.1073/pnas.0611659104
10.1186/1471-2180-12-S1-S2
10.1016/j.vetmic.2010.10.001
10.1126/science.1212782
10.1111/j.1574-6941.2011.01216.x
10.1128/AEM.30.6.893-896.1975
10.1111/j.1574-6941.2006.00249.x
10.1016/0022-2011(87)90127-3
10.1073/pnas.1202970109
10.1016/j.jip.2003.08.007
10.1007/s00248-011-9854-3
10.1111/j.1365-294X.2012.05496.x
10.1016/j.syapm.2009.08.002
10.1051/apido/2009065
10.1007/s00040-011-0194-6
10.3844/ajassp.2012.807.817
10.1371/journal.pone.0033188
10.1016/j.peptides.2004.03.016
10.1099/00221287-76-1-211
10.1126/science.1146498
10.1007/s00284-012-0186-4
ContentType Journal Article
Copyright COPYRIGHT 2013 Public Library of Science
2013. This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Competing Interests: The authors have declared that no competing interests exist.
Conceived and designed the experiments: SV KEA. Performed the experiments: SV. Analyzed the data: SV SMR KEA. Contributed reagents/materials/analysis tools: SV SMR KEA. Wrote the paper: SV SMR KEA.
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3749107/
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References ref56
E Crotti (ref64) 2009; 11
JG Lundgren (ref2) 2010; 5(5)
MC García (ref47) 2010; 2
RJ Dillon (ref63) 2004; 49
G Storelli (ref9) 2011; 14
MF Ramadan (ref44) 2012; 4
JD Thompson (ref37) 1994; 22
MM Aween (ref55) 2012; 9
H Koch (ref59) 2011; 62
KI Mohr (ref17) 2006; 8
M Gilliam (ref22) 1979; 10
TC Olofsson (ref58) 2008; 57
E Forsgren (ref11) 2010; 41
VG Martinson (ref14) 2012; 78
T Rodriguez-Navarro (ref50) 1973; 76
J Pain (ref10) 1966; 9
R Fontana (ref27) 2004; 25
A Endo (ref54) 2011; 62
M Gilliam (ref18) 1971; 4
TR Shamala (ref52) 2000; 30
M Gilliam (ref21) 1997; 155
ref42
NA Moran (ref1) 2007; 104
B Chouaia (ref7) 2012; 12
P Engel (ref39) 2012; 109
S Rauch (ref33) 2009; 75
JW McCreadie (ref5) 2005; 108
VG Martinson (ref15) 2011; 20
M Gilliam (ref23) 1979; 10
S Vojvodic (ref32) 2010; 149
T Disayathanoowat (ref60) 2012; 79
Q McFrederick (ref12) 2012; 21
ref34
CI Pavel (ref48) 2011; 44
ref31
ref30
SC Shin (ref8) 2011; 334
JR Liu (ref46) 2008; 56
ref38
A Jeyaprakash (ref61) 2003; 84
A Romanelli (ref45) 2011; 17
D Babendreier (ref57) 2007; 59
M Gilliam (ref19) 1987; 49
J-H Ryu (ref6) 2008; 319
DP Neveling (ref40) 2012; 65
J Simpson (ref65) 1955; 96
A Koeppel (ref43) 2008; 105
TA Hall (ref35) 1999; 41
K Bilikova (ref26) 2002; 528
T Rodriguez-Navarro (ref51) 1975; 30
JD Evans (ref20) 2006; 6
ref24
ref25
LR Batra (ref66) 1973; 49
A Vásquez (ref41) 2009; 40
JA Russell (ref3) 2009; 106
ref28
ref29
A Endo (ref53) 2009; 32
NA Moran (ref13) 2012; 4
M Katoh (ref36) 2002; 30
ref62
DL Cox-Foster (ref16) 2007; 318
KE Anderson (ref49) 2011; 58
EM Janson (ref4) 2008; 62
References_xml – volume: 4
  start-page: 315
  year: 1971
  ident: ref18
  article-title: Microbial sterility of the intestinal content of the immature honey bee Apis mellifera
  publication-title: Ann Entomol Sac Am
  doi: 10.1093/aesa/64.1.315
  contributor:
    fullname: M Gilliam
– volume: 17
  start-page: 348
  year: 2011
  ident: ref45
  article-title: Peptides from royal jelly: studies on the antimicrobial activity of jelleins, jelleins analogs and synergy with temporins
  publication-title: J Pept Sci
  doi: 10.1002/psc.1316
  contributor:
    fullname: A Romanelli
– volume: 106
  start-page: 21236
  year: 2009
  ident: ref3
  article-title: Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants
  publication-title: Proc Natl Acad Sci USA
  doi: 10.1073/pnas.0907926106
  contributor:
    fullname: JA Russell
– volume: 10
  start-page: 269
  year: 1979
  ident: ref23
  article-title: Microbiology of pollen and bee bread: the genus Bacillus
  publication-title: Apidologie
  doi: 10.1051/apido:19790304
  contributor:
    fullname: M Gilliam
– ident: ref30
  doi: 10.4159/9780674043404
– volume: 75
  start-page: 3344
  year: 2009
  ident: ref33
  article-title: Negative correlation between individual-insect-level virulence and colony-level virulence of Paenibacillus larvae, the etiological agent of American foulbrood of honeybees
  publication-title: Appl Environ Microbiol
  doi: 10.1128/AEM.02839-08
  contributor:
    fullname: S Rauch
– volume: 96
  start-page: 117
  year: 1955
  ident: ref65
  article-title: The significance of the presence of pollen in the food of worker larvae of the honey-bee
  publication-title: QJ Microsc Sci
  contributor:
    fullname: J Simpson
– ident: ref24
– volume: 319
  start-page: 777
  year: 2008
  ident: ref6
  article-title: Innate immune homeostasis by the homeobox gene Caudal and commensal-gut mutualism in Drosophila.
  publication-title: Science
  doi: 10.1126/science.1149357
  contributor:
    fullname: J-H Ryu
– volume: 11
  start-page: 3252
  year: 2009
  ident: ref64
  article-title: Asaia, a versatile acetic acid bacterial symbiont, capable of cross-colonizing insects of phylogenetically distant genera and orders. Environ
  publication-title: Microbiol
  contributor:
    fullname: E Crotti
– volume: 62
  start-page: 997
  year: 2008
  ident: ref4
  article-title: Phytophagous insectmicrobe mutualisms and adaptive evolutionary diversification
  publication-title: Evolution
  doi: 10.1111/j.1558-5646.2008.00348.x
  contributor:
    fullname: EM Janson
– volume: 20
  start-page: 619
  year: 2011
  ident: ref15
  article-title: A simple and distinctive microbiota associated with honey bees and bumble bees
  publication-title: Mol Ecol
  doi: 10.1111/j.1365-294X.2010.04959.x
  contributor:
    fullname: VG Martinson
– volume: 528
  start-page: 125
  year: 2002
  ident: ref26
  article-title: Apisimin, a new serine-valine-rich peptide from honeybee (Apis mellifera L.) royal jelly: purification and molecular characterization
  publication-title: FEBS Lett
  doi: 10.1016/S0014-5793(02)03272-6
  contributor:
    fullname: K Bilikova
– volume: 105
  start-page: 2504
  year: 2008
  ident: ref43
  article-title: Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics
  publication-title: Proc Natl Acad Sci USA
  doi: 10.1073/pnas.0712205105
  contributor:
    fullname: A Koeppel
– ident: ref62
  doi: 10.1371/journal.pone.0041250
– volume: 78
  start-page: 2830
  year: 2012
  ident: ref14
  article-title: Establishment of characteristic gut bacteria during development of the honey bee worker
  publication-title: Appl Environ Microbiol
  doi: 10.1128/AEM.07810-11
  contributor:
    fullname: VG Martinson
– volume: 22
  start-page: 4673
  year: 1994
  ident: ref37
  article-title: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/22.22.4673
  contributor:
    fullname: JD Thompson
– ident: ref34
– volume: 9
  start-page: 209
  year: 1966
  ident: ref10
  article-title: Recherches biochimiques et physiologiques sur le pollen emmagasine par les abeilles
  publication-title: Ann Abeille
  doi: 10.1051/apido:19660302
  contributor:
    fullname: J Pain
– volume: 14
  start-page: 403
  year: 2011
  ident: ref9
  article-title: Lactobacillus plantarum Promotes Drosophila Systemic Growth by Modulating Hormonal Signals through TOR-Dependent Nutrient Sensing
  publication-title: Cell Metabolism
  doi: 10.1016/j.cmet.2011.07.012
  contributor:
    fullname: G Storelli
– volume: 4
  start-page: e36393
  year: 2012
  ident: ref13
  article-title: Distinctive gut microbiota of honey bees assessed using deep sampling from Individual worker bees
  publication-title: PLoS ONE 7
  doi: 10.1371/journal.pone.0036393
  contributor:
    fullname: NA Moran
– volume: 6
  start-page: 4
  year: 2006
  ident: ref20
  article-title: Antagonistic interactions between honey bee bacterial symbionts and implications for disease
  publication-title: BMC Ecol
  doi: 10.1186/1472-6785-6-4
  contributor:
    fullname: JD Evans
– volume: 8
  start-page: 258
  year: 2006
  ident: ref17
  article-title: Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field
  publication-title: Environ Microbiol
  doi: 10.1111/j.1462-2920.2005.00893.x
  contributor:
    fullname: KI Mohr
– volume: 4
  start-page: 39
  year: 2012
  ident: ref44
  article-title: Bioactive compounds and health-promoting properties of royal jelly: A review
  publication-title: J Funct Food
  doi: 10.1016/j.jff.2011.12.007
  contributor:
    fullname: MF Ramadan
– volume: 5(5)
  start-page: e10831
  year: 2010
  ident: ref2
  article-title: Bacterial gut symbionts contribute to seed digestion in an omnivorous beetle
  publication-title: PLoS ONE
  doi: 10.1371/journal.pone.0010831
  contributor:
    fullname: JG Lundgren
– volume: 10
  start-page: 43
  year: 1979
  ident: ref22
  article-title: Microbiology of pollen and bee bread: the yeasts
  publication-title: Apidologie
  doi: 10.1051/apido:19790106
  contributor:
    fullname: M Gilliam
– volume: 155
  start-page: 1
  year: 1997
  ident: ref21
  article-title: Identification and roles of non-pathogenic microflora associated with honey bees
  publication-title: FEMS Microbiol Lett
  doi: 10.1016/S0378-1097(97)00337-6
  contributor:
    fullname: M Gilliam
– volume: 41
  start-page: 95
  year: 1999
  ident: ref35
  article-title: Bioedit: a user friendly biological sequence alignment editor and alignment program for Windows 95/98 NT
  publication-title: Nucleic Acid Symposium Series
  contributor:
    fullname: TA Hall
– volume: 30
  start-page: 3059
  year: 2002
  ident: ref36
  article-title: MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkf436
  contributor:
    fullname: M Katoh
– volume: 56
  start-page: 11447
  year: 2008
  ident: ref46
  article-title: Antioxidant properties of royal jelly associated with larval age and time of harvest
  publication-title: J Agricul Food Chem
  doi: 10.1021/jf802494e
  contributor:
    fullname: JR Liu
– volume: 62
  start-page: 500
  year: 2011
  ident: ref54
  article-title: Characterization and emended description of Lactobacillus kunkeei as a fructophilic lactic acid bacterium
  publication-title: Int J Syst Evol Microbiol
  doi: 10.1099/ijs.0.031054-0
  contributor:
    fullname: A Endo
– volume: 40
  start-page: 26
  year: 2009
  ident: ref41
  article-title: Scientific note on the lactic acid bacterial flora in honeybees in the USA – A comparison with bees from Sweden
  publication-title: Apidologie
  doi: 10.1051/apido:2008063
  contributor:
    fullname: A Vásquez
– volume: 49
  start-page: 71
  year: 2004
  ident: ref63
  article-title: The gut bacteria of insects: nonpathogenic interactions
  publication-title: Annu Rev Entomol
  doi: 10.1146/annurev.ento.49.061802.123416
  contributor:
    fullname: RJ Dillon
– volume: 108
  start-page: 362
  year: 2005
  ident: ref5
  article-title: Context dependent symbiosis between black flies (Diptera: Simuliidae) and trichomycete fungi (Harpellales: Legeriomycetaceae)
  publication-title: Oikos
  doi: 10.1111/j.0030-1299.2005.13417.x
  contributor:
    fullname: JW McCreadie
– volume: 2
  start-page: 93
  year: 2010
  ident: ref47
  article-title: Antibacterial activity of Royal Jelly against bacteria capable of infecting cutaneous wounds
  publication-title: Journal of ApiProduct and ApiMedical Science
  doi: 10.3896/IBRA.4.02.3.02
  contributor:
    fullname: MC García
– volume: 30
  start-page: 453
  year: 2000
  ident: ref52
  article-title: Stimulatory effect of honey on multiplication of lactic acid bacteria under in vitro and in vivo conditions
  publication-title: Lett Appl Microbiol
  doi: 10.1046/j.1472-765x.2000.00746.x
  contributor:
    fullname: TR Shamala
– volume: 57
  start-page: 356
  year: 2008
  ident: ref58
  article-title: Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera
  publication-title: Curr Microbiol
  doi: 10.1007/s00284-008-9202-0
  contributor:
    fullname: TC Olofsson
– volume: 104
  start-page: 8627
  year: 2007
  ident: ref1
  article-title: Symbiosis as an adaptive process and source of phenotypic complexity
  publication-title: Proc Natl Acad Sci USA
  doi: 10.1073/pnas.0611659104
  contributor:
    fullname: NA Moran
– volume: 12
  start-page: S2
  year: 2012
  ident: ref7
  article-title: Delayed larval development in Anopheles mosquitoes deprived of Asaia bacterial symbionts
  publication-title: BMC Microbiol
  doi: 10.1186/1471-2180-12-S1-S2
  contributor:
    fullname: B Chouaia
– volume: 149
  start-page: 200
  year: 2010
  ident: ref32
  article-title: Opposing temperature-dependent mortality after infection with an obligate and facultative fungal pathogen of honeybees
  publication-title: Vet Microbiol
  doi: 10.1016/j.vetmic.2010.10.001
  contributor:
    fullname: S Vojvodic
– ident: ref29
– volume: 334
  start-page: 670
  year: 2011
  ident: ref8
  article-title: Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling
  publication-title: Science
  doi: 10.1126/science.1212782
  contributor:
    fullname: SC Shin
– volume: 79
  start-page: 273
  year: 2012
  ident: ref60
  article-title: T-RFLP analysis of bacterial communities in the midguts of Apis mellifera and Apis cerana honey bees in Thailand
  publication-title: FEMS Microbiol Ecol
  doi: 10.1111/j.1574-6941.2011.01216.x
  contributor:
    fullname: T Disayathanoowat
– volume: 30
  start-page: 893
  year: 1975
  ident: ref51
  article-title: Microbiology of ripening honey
  publication-title: Appl Microbiol
  doi: 10.1128/AEM.30.6.893-896.1975
  contributor:
    fullname: T Rodriguez-Navarro
– ident: ref25
– volume: 44
  start-page: 108
  year: 2011
  ident: ref48
  article-title: Biological Activities of Royal Jelly – Review. Animal Science and Biotechnologies
  contributor:
    fullname: CI Pavel
– volume: 59
  start-page: 600
  year: 2007
  ident: ref57
  article-title: Bacterial community structures in honeybee intestines and their response to two insecticidal proteins
  publication-title: FEMS Microbiol Ecol
  doi: 10.1111/j.1574-6941.2006.00249.x
  contributor:
    fullname: D Babendreier
– volume: 49
  start-page: 70
  year: 1987
  ident: ref19
  article-title: Microbiology of feces of the larval honey bee, Apis mellifera
  publication-title: J Invertebr Pathol
  doi: 10.1016/0022-2011(87)90127-3
  contributor:
    fullname: M Gilliam
– volume: 109
  start-page: 11002
  year: 2012
  ident: ref39
  article-title: Functional diversity within the simple gut microbiota of the honey bee
  publication-title: Proc Natl Acad Sci USA
  doi: 10.1073/pnas.1202970109
  contributor:
    fullname: P Engel
– ident: ref38
– volume: 84
  start-page: 96
  year: 2003
  ident: ref61
  article-title: Bacterial diversity in worker adults of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) assessed using 16S rRNA sequences
  publication-title: J Invertebr Pathol
  doi: 10.1016/j.jip.2003.08.007
  contributor:
    fullname: A Jeyaprakash
– volume: 62
  start-page: 121
  year: 2011
  ident: ref59
  article-title: Bacterial communities in central European bumblebees: low diversity and high specificity
  publication-title: Microb Ecol
  doi: 10.1007/s00248-011-9854-3
  contributor:
    fullname: H Koch
– volume: 21
  start-page: 1754
  year: 2012
  ident: ref12
  article-title: Environment or kin: whence do bees obtain acidophilic bacteria?
  publication-title: Mol Ecol
  doi: 10.1111/j.1365-294X.2012.05496.x
  contributor:
    fullname: Q McFrederick
– ident: ref28
– ident: ref42
– volume: 32
  start-page: 593
  year: 2009
  ident: ref53
  article-title: Isolation and characterization of fructophilic lactic acid bacteria from fructose-rich niches
  publication-title: Syst Appl Microbiol
  doi: 10.1016/j.syapm.2009.08.002
  contributor:
    fullname: A Endo
– volume: 41
  start-page: 99
  year: 2010
  ident: ref11
  article-title: Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae
  publication-title: Apidologie
  doi: 10.1051/apido/2009065
  contributor:
    fullname: E Forsgren
– volume: 58
  start-page: 431
  year: 2011
  ident: ref49
  article-title: An emerging paradigm of colony health: microbial balance of the honey bee and hive (Apis mellifera)
  publication-title: Insectes Sociaux
  doi: 10.1007/s00040-011-0194-6
  contributor:
    fullname: KE Anderson
– volume: 9
  start-page: 807
  year: 2012
  ident: ref55
  article-title: Evaluating on antibacterial activity of Lactobacillus acidophilus strains isolated from honey
  publication-title: Am J Applied Sci
  doi: 10.3844/ajassp.2012.807.817
  contributor:
    fullname: MM Aween
– ident: ref56
  doi: 10.1371/journal.pone.0033188
– volume: 49
  start-page: 13
  year: 1973
  ident: ref66
  article-title: The mycoflora of domesticated and wild bees (Apoidea)
  publication-title: Mycopathologia
  contributor:
    fullname: LR Batra
– volume: 25
  start-page: 919
  year: 2004
  ident: ref27
  article-title: Jelleines: a family of antimicrobial peptides from the royal jelly of honeybees (Apis mellifera).
  publication-title: Peptides
  doi: 10.1016/j.peptides.2004.03.016
  contributor:
    fullname: R Fontana
– volume: 76
  start-page: 211
  year: 1973
  ident: ref50
  article-title: Gluconic acid producing bacteria from honey bee and ripening honey
  publication-title: J Gen Microbiol
  doi: 10.1099/00221287-76-1-211
  contributor:
    fullname: T Rodriguez-Navarro
– volume: 318
  start-page: 283
  year: 2007
  ident: ref16
  article-title: A metagenomic survey of microbes in honey bee colony collapse disorder
  publication-title: Science
  doi: 10.1126/science.1146498
  contributor:
    fullname: DL Cox-Foster
– volume: 65
  start-page: 507
  year: 2012
  ident: ref40
  article-title: Fructophilic Lactobacillus kunkeei and Lactobacillus brevis isolated from fresh flowers, bees and bee-hives
  publication-title: Curr Microbiol
  doi: 10.1007/s00284-012-0186-4
  contributor:
    fullname: DP Neveling
– ident: ref31
SSID ssj0053866
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Snippet The first step in understanding gut microbial ecology is determining the presence and potential niche breadth of associated microbes. While the core gut...
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SourceType Open Website
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Index Database
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StartPage e72106
SubjectTerms Acetobacteraceae
Acetobacteraceae - genetics
Acetobacteraceae - physiology
Acids
Adults
Africa
Animals
Apis mellifera
Bacteria
Bacteria - classification
Bacteria - genetics
Bacteria - isolation & purification
bacterial communities
Bees
Bees - microbiology
Biodiversity
Biology
digestive system
disease course
Disease resistance
DNA Barcoding, Taxonomic
DNA, Bacterial - chemistry
DNA, Bacterial - genetics
Ecology
Europe
European honeybee
Evolutionary biology
Firmicutes
Flora
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Fungi
Gastrointestinal Tract - microbiology
Genetic Variation
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honey bees
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insect larvae
Insects
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Intestinal microflora
intestinal microorganisms
Lactobacillus
Lactobacillus - genetics
Lactobacillus - physiology
Larva - microbiology
Larvae
Microbiota
Microbiota (Symbiotic organisms)
Microorganisms
Molecular Sequence Data
Neisseriaceae
Neisseriaceae - genetics
Neisseriaceae - physiology
Niche breadth
Nutrition
Physiology
Pollinators
RNA, Ribosomal, 16S - genetics
Royal jelly
Sequence Analysis, DNA
Studies
Symbiosis
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Title Microbial Gut Diversity of Africanized and European Honey Bee Larval Instars
URI https://www.ncbi.nlm.nih.gov/pubmed/23991051
https://www.proquest.com/docview/1430787236
https://search.proquest.com/docview/1429215219
https://pubmed.ncbi.nlm.nih.gov/PMC3749107
https://doaj.org/article/5a05978afdbc4a90b935bbd42e7ab716
http://dx.doi.org/10.1371/journal.pone.0072106
Volume 8
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