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Title: Distinctive Gut Microbiota of Honey Bees Assessed Using Deep Sampling from Individual Worker Bees

Abstract

Surveys of 16S rDNA sequences from the honey bee, Apis mellifera, have revealed the presence of eight distinctive bacterial phylotypes in intestinal tracts of adult worker bees. Because previous studies have been limited to relatively few sequences from samples pooled from multiple hosts, the extent of variation in this microbiota among individuals within and between colonies and locations has been unclear. We surveyed the gut microbiota of 40 individual workers from two sites, Arizona and Maryland USA, sampling four colonies per site. Universal primers were used to amplify regions of 16S ribosomal RNA genes, and amplicons were sequenced using 454 pyrotag methods, enabling analysis of about 330,000 bacterial reads. Over 99% of these sequences belonged to clusters for which the first blastn hits in GenBank were members of the known bee phylotypes. Four phylotypes, one within Gammaproteobacteria (corresponding to ‘‘Candidatus Gilliamella apicola’’) one within Betaproteobacteria (‘‘Candidatus Snodgrassella alvi’’), and two within Lactobacillus, were present in every bee, though their frequencies varied. The same typical bacterial phylotypes were present in all colonies and at both sites. Community profiles differed significantly among colonies and between sites, mostly due to the presence in some Arizona colonies of two species of Enterobacteriaceae not retrievedmore » previously from bees. Analysis of Sanger sequences of rRNA of the Snodgrassella and Gilliamella phylotypes revealed that single bees contain numerous distinct strains of each phylotype. Strains showed some differentiation between localities, especially for the Snodgrassella phylotype.« less

Authors:
 [1];  [1];  [1];  [1]
  1. Yale Univ., New Haven, CT (United States). Dept. of Ecology and Evolutionary Biology
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1627515
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 7; Journal Issue: 4; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics

Citation Formats

Moran, Nancy A., Hansen, Allison K., Powell, J. Elijah, and Sabree, Zakee L. Distinctive Gut Microbiota of Honey Bees Assessed Using Deep Sampling from Individual Worker Bees. United States: N. p., 2012. Web. doi:10.1371/journal.pone.0036393.
Moran, Nancy A., Hansen, Allison K., Powell, J. Elijah, & Sabree, Zakee L. Distinctive Gut Microbiota of Honey Bees Assessed Using Deep Sampling from Individual Worker Bees. United States. https://doi.org/10.1371/journal.pone.0036393
Moran, Nancy A., Hansen, Allison K., Powell, J. Elijah, and Sabree, Zakee L. Fri . "Distinctive Gut Microbiota of Honey Bees Assessed Using Deep Sampling from Individual Worker Bees". United States. https://doi.org/10.1371/journal.pone.0036393. https://www.osti.gov/servlets/purl/1627515.
@article{osti_1627515,
title = {Distinctive Gut Microbiota of Honey Bees Assessed Using Deep Sampling from Individual Worker Bees},
author = {Moran, Nancy A. and Hansen, Allison K. and Powell, J. Elijah and Sabree, Zakee L.},
abstractNote = {Surveys of 16S rDNA sequences from the honey bee, Apis mellifera, have revealed the presence of eight distinctive bacterial phylotypes in intestinal tracts of adult worker bees. Because previous studies have been limited to relatively few sequences from samples pooled from multiple hosts, the extent of variation in this microbiota among individuals within and between colonies and locations has been unclear. We surveyed the gut microbiota of 40 individual workers from two sites, Arizona and Maryland USA, sampling four colonies per site. Universal primers were used to amplify regions of 16S ribosomal RNA genes, and amplicons were sequenced using 454 pyrotag methods, enabling analysis of about 330,000 bacterial reads. Over 99% of these sequences belonged to clusters for which the first blastn hits in GenBank were members of the known bee phylotypes. Four phylotypes, one within Gammaproteobacteria (corresponding to ‘‘Candidatus Gilliamella apicola’’) one within Betaproteobacteria (‘‘Candidatus Snodgrassella alvi’’), and two within Lactobacillus, were present in every bee, though their frequencies varied. The same typical bacterial phylotypes were present in all colonies and at both sites. Community profiles differed significantly among colonies and between sites, mostly due to the presence in some Arizona colonies of two species of Enterobacteriaceae not retrieved previously from bees. Analysis of Sanger sequences of rRNA of the Snodgrassella and Gilliamella phylotypes revealed that single bees contain numerous distinct strains of each phylotype. Strains showed some differentiation between localities, especially for the Snodgrassella phylotype.},
doi = {10.1371/journal.pone.0036393},
journal = {PLoS ONE},
number = 4,
volume = 7,
place = {United States},
year = {Fri Apr 27 00:00:00 EDT 2012},
month = {Fri Apr 27 00:00:00 EDT 2012}
}

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Do Honeybees Shape the Bacterial Community Composition in Floral Nectar?
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Microbial Gut Diversity of Africanized and European Honey Bee Larval Instars
journal, August 2013


Honey Bees Avoid Nectar Colonized by Three Bacterial Species, But Not by a Yeast Species, Isolated from the Bee Gut
journal, January 2014


Modulation of the honey bee queen microbiota: Effects of early social contact
journal, July 2018


Temporal changes in the viromes of Swedish Varroa-resistant and Varroa-susceptible honeybee populations
journal, December 2018


Acquisition and Structuring of Midgut Bacterial Communities in Gypsy Moth (Lepidoptera: Erebidae) Larvae
journal, June 2014

  • Mason, Charles J.; Raffa, Kenneth F.
  • Environmental Entomology, Vol. 43, Issue 3
  • DOI: 10.1603/en14031

Characterization of the Core and Caste-Specific Microbiota in the Termite, Reticulitermes flavipes
journal, February 2016


Honey Bee Gut Microbiome Is Altered by In-Hive Pesticide Exposures
journal, August 2016

  • Kakumanu, Madhavi L.; Reeves, Alison M.; Anderson, Troy D.
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.01255

Exploring Interactions between the Gut Microbiota and Social Behavior through Nutrition
journal, November 2018

  • Pasquaretta, Cristian; Gómez-Moracho, Tamara; Heeb, Philipp
  • Genes, Vol. 9, Issue 11
  • DOI: 10.3390/genes9110534

Gut microbiota composition is associated with environmental landscape in honey bees
journal, November 2017

  • Jones, Julia C.; Fruciano, Carmelo; Hildebrand, Falk
  • Ecology and Evolution, Vol. 8, Issue 1
  • DOI: 10.1002/ece3.3597

Bacterial communities associated with honeybee food stores are correlated with land use
journal, April 2018

  • Donkersley, Philip; Rhodes, Glenn; Pickup, Roger W.
  • Ecology and Evolution, Vol. 8, Issue 10
  • DOI: 10.1002/ece3.3999

Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus)
journal, April 2014

  • Cariveau, Daniel P.; Elijah Powell, J.; Koch, Hauke
  • The ISME Journal, Vol. 8, Issue 12
  • DOI: 10.1038/ismej.2014.68

Characterisation of the British honey bee metagenome
journal, November 2018


Functional diversity within the simple gut microbiota of the honey bee
journal, June 2012

  • Engel, P.; Martinson, V. G.; Moran, N. A.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 27
  • DOI: 10.1073/pnas.1202970109

Genomics and host specialization of honey bee and bumble bee gut symbionts
journal, July 2014

  • Kwong, W. K.; Engel, P.; Koch, H.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 31
  • DOI: 10.1073/pnas.1405838111

Glyphosate perturbs the gut microbiota of honey bees
journal, September 2018

  • Motta, Erick V. S.; Raymann, Kasie; Moran, Nancy A.
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 41
  • DOI: 10.1073/pnas.1803880115

Evolution of host specialization in gut microbes: the bee gut as a model
journal, May 2015


Lactobacillus micheneri sp. nov., Lactobacillus timberlakei sp. nov. and Lactobacillus quenuiae sp. nov., lactic acid bacteria isolated from wild bees and flowers
journal, June 2018

  • McFrederick, Quinn S.; Vuong, Hoang Q.; Rothman, Jason A.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 68, Issue 6
  • DOI: 10.1099/ijsem.0.002758

Characterisation of the UK honey bee (Apis mellifera) metagenome
posted_content, May 2018

  • Regan, Tim; Barnett, Mark W.; Laetsch, Dominik R.
  • bioRxiv
  • DOI: 10.1101/293647

The honey bee gut microbiota: strategies for study and characterization: Studying the Honey Bee Gut Microbiota
journal, February 2019

  • Romero, S.; Nastasa, A.; Chapman, A.
  • Insect Molecular Biology, Vol. 28, Issue 4
  • DOI: 10.1111/imb.12567

Antibiotics reduce genetic diversity of core species in the honeybee gut microbiome
journal, December 2017

  • Raymann, Kasie; Bobay, Louis-Marie; Moran, Nancy A.
  • Molecular Ecology, Vol. 27, Issue 8
  • DOI: 10.1111/mec.14434

Long-Term Exposure to Antibiotics Has Caused Accumulation of Resistance Determinants in the Gut Microbiota of Honeybees
journal, December 2012


Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut
journal, April 2015


Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees
journal, March 2017


Metagenomic Detection of Viral Pathogens in Spanish Honeybees: Co-Infection by Aphid Lethal Paralysis, Israel Acute Paralysis and Lake Sinai Viruses
journal, February 2013


A Cross-Taxon Analysis of Insect-Associated Bacterial Diversity
journal, April 2013


Glyphosate, but not its metabolite AMPA, alters the honeybee gut microbiota
journal, April 2019


Honey bee microbiome associated with different hive and sample types over a honey production season
journal, November 2019


The different dietary sugars modulate the composition of the gut microbiota in honeybee during overwintering
posted_content, March 2020


Beyond 16S rRNA Community Profiling: Intra-Species Diversity in the Gut Microbiota
journal, September 2016


Pyrosequencing Reveals the Predominance of Pseudomonadaceae in Gut Microbiome of a Gall Midge
journal, June 2014


The Anopheles Mosquito Microbiota and Their Impact on Pathogen Transmission
book, July 2013

  • Gendrin, Mathilde; Christophides, George K.
  • Anopheles mosquitoes - New insights into malaria vectors
  • DOI: 10.5772/55107

Biology of Paenibacillus larvae, a deadly pathogen of honey bee larvae
journal, July 2016

  • Ebeling, Julia; Knispel, Henriette; Hertlein, Gillian
  • Applied Microbiology and Biotechnology, Vol. 100, Issue 17
  • DOI: 10.1007/s00253-016-7716-0

Differential carbohydrate utilization and organic acid production by honey bee symbionts
journal, April 2018

  • Lee, Frederick J.; Miller, Kayla I.; Mckinlay, James B.
  • FEMS Microbiology Ecology
  • DOI: 10.1101/294249

Diet-related gut bacterial dysbiosis correlates with impaired development, increased mortality and Nosema disease in the honeybee ( Apis mellifera )
journal, October 2016

  • Maes, Patrick W.; Rodrigues, Pedro A. P.; Oliver, Randy
  • Molecular Ecology, Vol. 25, Issue 21
  • DOI: 10.1111/mec.13862

Dynamic microbiome evolution in social bees
journal, March 2017

  • Kwong, Waldan K.; Medina, Luis A.; Koch, Hauke
  • Science Advances, Vol. 3, Issue 3
  • DOI: 10.1126/sciadv.1600513

Overlapping Community Compositions of Gut and Fecal Microbiomes in Lab-Reared and Field-Collected German Cockroaches
journal, June 2018

  • Kakumanu, Madhavi L.; Maritz, Julia M.; Carlton, Jane M.
  • Applied and Environmental Microbiology, Vol. 84, Issue 17
  • DOI: 10.1128/aem.01037-18

The hologenome concept of evolution after 10 years
journal, April 2018


The different dietary sugars modulate the composition of the gut microbiota in honeybee during overwintering
posted_content, March 2020


Impact of beneficial bacteria supplementation on the gut microbiota, colony development and productivity of Apis mellifera L.
journal, February 2018

  • Alberoni, D.; Baffoni, L.; Gaggìa, F.
  • Beneficial Microbes, Vol. 9, Issue 2
  • DOI: 10.3920/bm2017.0061

Gut and Whole-Body Microbiota of the Honey Bee Separate Thriving and Non-thriving Hives
journal, November 2018


Genomic Signatures of Honey Bee Association in an Acetic Acid Symbiont
journal, September 2020

  • Smith, Eric A.; Newton, Irene L. G.
  • Genome Biology and Evolution, Vol. 12, Issue 10
  • DOI: 10.1093/gbe/evaa183

Addressing the diversity of the honeybee gut symbiont Gilliamella: description of Gilliamella apis sp. nov., isolated from the gut of honeybees (Apis mellifera)
journal, May 2018

  • Ludvigsen, Jane; Porcellato, Davide; Amdam, Gro V.
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 68, Issue 5
  • DOI: 10.1099/ijsem.0.002749

Disentangling metabolic functions of bacteria in the honey bee gut
posted_content, July 2017

  • Kešnerová, Lucie; Mars, Ruben A. T.; Ellegaard, Kirsten M.
  • bioRxiv
  • DOI: 10.1101/157461

Coral microbiome database: Integration of sequences reveals high diversity and relatedness of coral‐associated microbes
journal, September 2018

  • Huggett, Megan J.; Apprill, Amy
  • Environmental Microbiology Reports, Vol. 11, Issue 3
  • DOI: 10.1111/1758-2229.12686

Standard methods for research on Apis mellifera gut symbionts
journal, January 2013

  • Engel, Philipp; James, Rosalind R.; Koga, Ryuichi
  • Journal of Apicultural Research, Vol. 52, Issue 4
  • DOI: 10.3896/ibra.1.52.4.07

Antibiotic treatment impairs protein digestion in the honeybee, Apis mellifera
journal, December 2019


Erratum: Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus)
journal, November 2014

  • Cariveau, Daniel P.; Elijah Powell, J.; Koch, Hauke
  • The ISME Journal, Vol. 8, Issue 12
  • DOI: 10.1038/ismej.2014.180

Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria
journal, January 2016

  • Kešnerová, Lucie; Moritz, Roxane; Engel, Philipp
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 1
  • DOI: 10.1099/ijsem.0.000736

Microbiome Structure Influences Infection by the Parasite Crithidia bombi in Bumble Bees
journal, January 2018

  • Mockler, Blair K.; Kwong, Waldan K.; Moran, Nancy A.
  • Applied and Environmental Microbiology, Vol. 84, Issue 7
  • DOI: 10.1128/aem.02335-17

The Bacterial Communities Associated with Honey Bee (Apis mellifera) Foragers
journal, April 2014


Caste-Specific Differences in Hindgut Microbial Communities of Honey Bees (Apis mellifera)
journal, April 2015


The gut bacterial communities across six grasshopper species from a coastal tallgrass prairie
journal, January 2020


Metatranscriptomic analyses of honey bee colonies
journal, March 2015


Hibernation Leads to Altered Gut Communities in Bumblebee Queens (Bombus terrestris)
journal, December 2018


Caterpillars lack a resident gut microbiome
journal, August 2017

  • Hammer, Tobin J.; Janzen, Daniel H.; Hallwachs, Winnie
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 36
  • DOI: 10.1073/pnas.1707186114

Host species and developmental stage, but not host social structure, affects bacterial community structure in socially polymorphic bees
journal, March 2014

  • McFrederick, Quinn S.; Wcislo, William T.; Hout, Michael C.
  • FEMS Microbiology Ecology, Vol. 88, Issue 2
  • DOI: 10.1111/1574-6941.12302

Bacterial communities associated with honeybee food stores are correlated with land use
journal, April 2018

  • Donkersley, Philip; Rhodes, Glenn; Pickup, Roger W.
  • Ecology and Evolution, Vol. 8, Issue 10
  • DOI: 10.1002/ece3.3999

Gut bacterial and fungal communities of the domesticated silkworm (Bombyx mori) and wild mulberry-feeding relatives
journal, June 2018


Gut microbiota structure differs between honeybees in winter and summer
journal, December 2019


Genomic diversity landscape of the honey bee gut microbiota
journal, January 2019


16S rRNA sequencing reveals likely beneficial core microbes within faecal samples of the EU protected slug Geomalacus maculosus
journal, July 2018


Intensity of Nosema ceranae infection is associated with specific honey bee gut bacteria and weakly associated with gut microbiome structure
journal, March 2019


Forager bees (Apis mellifera) highly express immune and detoxification genes in tissues associated with nectar processing
journal, November 2015

  • Vannette, Rachel L.; Mohamed, Abbas; Johnson, Brian R.
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep16224

Glyphosate perturbs the gut microbiota of honey bees
journal, September 2018

  • Motta, Erick V. S.; Raymann, Kasie; Moran, Nancy A.
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 41
  • DOI: 10.1073/pnas.1803880115

Evolution of host specialization in gut microbes: the bee gut as a model
journal, May 2015


Winding paths to simplicity: genome evolution in facultative insect symbionts
journal, August 2016

  • Lo, Wen-Sui; Huang, Ya-Yi; Kuo, Chih-Horng
  • FEMS Microbiology Reviews, Vol. 40, Issue 6
  • DOI: 10.1093/femsre/fuw028

Functionally Structured Genomes in Lactobacillus kunkeei Colonizing the Honey Crop and Food Products of Honeybees and Stingless Bees
journal, May 2015

  • Tamarit, Daniel; Ellegaard, Kirsten M.; Wikander, Johan
  • Genome Biology and Evolution, Vol. 7, Issue 6
  • DOI: 10.1093/gbe/evv079

Dynamic microbiome evolution in social bees
journal, March 2017

  • Kwong, Waldan K.; Medina, Luis A.; Koch, Hauke
  • Science Advances, Vol. 3, Issue 3
  • DOI: 10.1126/sciadv.1600513

Overlapping Community Compositions of Gut and Fecal Microbiomes in Lab-Reared and Field-Collected German Cockroaches
journal, June 2018

  • Kakumanu, Madhavi L.; Maritz, Julia M.; Carlton, Jane M.
  • Applied and Environmental Microbiology, Vol. 84, Issue 17
  • DOI: 10.1128/aem.01037-18

Draft Genome Sequences of Four Parasaccharibacter apium Strains Isolated from Honey Bees
journal, March 2018


Genome Sequences of Lactobacillus sp. Strains wkB8 and wkB10, Members of the Firm-5 Clade, from Honey Bee Guts
journal, December 2014

  • Kwong, Waldan K.; Mancenido, Amanda L.; Moran, Nancy A.
  • Genome Announcements, Vol. 2, Issue 6
  • DOI: 10.1128/genomea.01176-14

Long-Term Exposure to Antibiotics Has Caused Accumulation of Resistance Determinants in the Gut Microbiota of Honeybees
journal, December 2012


Metabolism of Toxic Sugars by Strains of the Bee Gut Symbiont Gilliamella apicola
journal, November 2016


Diversification of Type VI Secretion System Toxins Reveals Ancient Antagonism among Bee Gut Microbes
journal, December 2017

  • Steele, Margaret I.; Kwong, Waldan K.; Whiteley, Marvin
  • mBio, Vol. 8, Issue 6
  • DOI: 10.1128/mbio.01630-17

Correction for Raymann et al., “Pathogenicity of Serratia marcescens Strains in Honey Bees”
journal, February 2019


RNAi and Antiviral Defense in the Honey Bee
journal, January 2015

  • Brutscher, Laura M.; Flenniken, Michelle L.
  • Journal of Immunology Research, Vol. 2015
  • DOI: 10.1155/2015/941897

The effect of training set on the classification of honey bee gut microbiota using the Naïve Bayesian Classifier
journal, January 2012


Analysis of the gut microbiota of walking sticks (Phasmatodea)
journal, September 2013


Draft genome sequences of two Bifidobacterium sp. from the honey bee (Apis mellifera)
journal, January 2013

  • Anderson, Kirk E.; Johansson, Andreas; Sheehan, Tim H.
  • Gut Pathogens, Vol. 5, Issue 1
  • DOI: 10.1186/1757-4749-5-42

Microbial composition of spiny ants (Hymenoptera: Formicidae: Polyrhachis) across their geographic range
journal, April 2017

  • Ramalho, Manuela Oliveira; Bueno, Odair Correa; Moreau, Corrie Saux
  • BMC Evolutionary Biology, Vol. 17, Issue 1
  • DOI: 10.1186/s12862-017-0945-8

Extensive intra-phylotype diversity in lactobacilli and bifidobacteria from the honeybee gut
journal, April 2015


Deep divergence and rapid evolutionary rates in gut-associated Acetobacteraceae of ants
journal, July 2016


In-hive variation of the gut microbial composition of honey bee larvae and pupae from the same oviposition time
journal, May 2019


The hologenome concept of evolution after 10 years
journal, April 2018


The queen’s gut refines with age: longevity phenotypes in a social insect model
journal, June 2018


Shifts in the Midgut/Pyloric Microbiota Composition within a Honey Bee Apiary throughout a Season
journal, January 2015

  • Ludvigsen, Jane; Rangberg, Anbjørg; Avershina, Ekaterina
  • Microbes and Environments, Vol. 30, Issue 3
  • DOI: 10.1264/jsme2.me15019

Antibiotic exposure perturbs the gut microbiota and elevates mortality in honeybees
journal, March 2017


Hidden Diversity in Honey Bee Gut Symbionts Detected by Single-Cell Genomics
journal, September 2014


Independent Studies Using Deep Sequencing Resolve the Same Set of Core Bacterial Species Dominating Gut Communities of Honey Bees
journal, July 2012


The Prevalence of Parasites and Pathogens in Asian Honeybees Apis cerana in China
journal, November 2012


Do Honeybees Shape the Bacterial Community Composition in Floral Nectar?
journal, July 2013


A Metatranscriptomic Approach to the Identification of Microbiota Associated with the Ant Formica exsecta
journal, November 2013


Honey Bees Avoid Nectar Colonized by Three Bacterial Species, But Not by a Yeast Species, Isolated from the Bee Gut
journal, January 2014


The Bacterial Communities Associated with Honey Bee (Apis mellifera) Foragers
journal, April 2014


Variation in Honey Bee Gut Microbial Diversity Affected by Ontogenetic Stage, Age and Geographic Location
journal, March 2015


Caste-Specific Differences in Hindgut Microbial Communities of Honey Bees (Apis mellifera)
journal, April 2015


Honey bee microbiome associated with different hive and sample types over a honey production season
journal, November 2019


The gut bacterial communities across six grasshopper species from a coastal tallgrass prairie
journal, January 2020


The different dietary sugars modulate the composition of the gut microbiota in honeybee during overwintering
posted_content, March 2020


Pyrosequencing 16S rRNA genes of bacteria associated with wild tiger mosquito Aedes albopictus: a pilot study
journal, May 2014

  • Minard, Guillaume; Tran, Florence-Hélène; Dubost, Audrey
  • Frontiers in Cellular and Infection Microbiology, Vol. 4
  • DOI: 10.3389/fcimb.2014.00059

Metatranscriptomic analyses of honey bee colonies
journal, March 2015


Characterization of the Core and Caste-Specific Microbiota in the Termite, Reticulitermes flavipes
journal, February 2016


Honey Bee Gut Microbiome Is Altered by In-Hive Pesticide Exposures
journal, August 2016

  • Kakumanu, Madhavi L.; Reeves, Alison M.; Anderson, Troy D.
  • Frontiers in Microbiology, Vol. 7
  • DOI: 10.3389/fmicb.2016.01255

Effect of Different Lignocellulosic Diets on Bacterial Microbiota and Hydrolytic Enzyme Activities in the Gut of the Cotton Boll Weevil (Anthonomus grandis)
journal, December 2016

  • Ben Guerrero, Emiliano; Soria, Marcelo; Salvador, Ricardo
  • Frontiers in Microbiology, Vol. 07
  • DOI: 10.3389/fmicb.2016.02093

Exploring Interactions between the Gut Microbiota and Social Behavior through Nutrition
journal, November 2018

  • Pasquaretta, Cristian; Gómez-Moracho, Tamara; Heeb, Philipp
  • Genes, Vol. 9, Issue 11
  • DOI: 10.3390/genes9110534

Pyrosequencing Reveals the Predominance of Pseudomonadaceae in Gut Microbiome of a Gall Midge
journal, June 2014


Disentangling metabolic functions of bacteria in the honey bee gut
text, January 2018


No apparent correlation between honey bee forager gut microbiota and honey production
journal, October 2015

  • Horton, Melissa A.; Oliver, Randy; Newton, Irene L.
  • PeerJ, Vol. 3
  • DOI: 10.7717/peerj.1329