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The Bee Microbiome: Impact on Bee Health and Model for Evolution and Ecology of Host-Microbe Interactions

Philipp Engel, Waldan K. Kwong, Quinn McFrederick, Kirk E. Anderson, Seth Michael Barribeau, James Angus Chandler, R. Scott Cornman, Jacques Dainat, Joachim R. de Miranda, Vincent Doublet, Olivier Emery, Jay D. Evans, Laurent Farinelli, Michelle L. Flenniken, Fredrik Granberg, Juris A. Grasis, Laurent Gauthier, Juliette Hayer, Hauke Koch, Sarah Kocher, Vincent G. Martinson, Nancy Moran, Monica Munoz-Torres, Irene Newton, Robert J. Paxton, Eli Powell, Ben M. Sadd, Paul Schmid-Hempel, Regula Schmid-Hempel, Se Jin Song, Ryan S. Schwarz, Dennis vanEngelsdorp, Benjamin Dainat
Gregory B. Hurst, Invited Editor, R. John Collier, Editor
Philipp Engel
aDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
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Waldan K. Kwong
bEcology and Evolutionary Biology, Yale University, New Haven, Connecticut, USA
cDepartment of Integrative Biology, University of Texas at Austin, Austin, Texas, USA
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Quinn McFrederick
dDepartment of Entomology, University of California, Riverside, California, USA
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Kirk E. Anderson
eUSDA, Carl Hayden Bee Research Center, Tucson, Arizona, USA
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Seth Michael Barribeau
fDepartment of Biology, East Carolina University, Greenville, North Carolina, USA
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James Angus Chandler
gDepartment of Microbiology, California Academy of Sciences, San Francisco, California, USA
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R. Scott Cornman
hU.S. Geological Survey, Fort Collins Science Center, Fort Collins, Colorado, USA
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Jacques Dainat
iBioinformatics Infrastructure for Life Sciences (BILS), Linköpings Universitet Victoria Westling, Linköping, Sweden, and Department of Medical Biochemistry and Microbiology Uppsala University, Uppsala, Sweden
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Joachim R. de Miranda
jDepartment of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden
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  • ORCID record for Joachim R. de Miranda
Vincent Doublet
kInstitute for Biology, Martin Luther University Halle-Wittenberg, Halle, Germany
lGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
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Olivier Emery
aDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
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Jay D. Evans
mUSDA, ARS Bee Research Laboratory, Beltsville, Maryland, USA
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Laurent Farinelli
nFasteris SA, Plan -les-Ouates, Switzerland
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Michelle L. Flenniken
oDepartment of Plant Sciences and Plant Pathology, Montana State University, Bozeman, Montana, USA
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Fredrik Granberg
pSLU, BVF, Virologi, Uppsala, Sweden
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Juris A. Grasis
qDepartment of Biology, North Life Sciences, San Diego State University, San Diego, California, USA
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Laurent Gauthier
aDepartment of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
bEcology and Evolutionary Biology, Yale University, New Haven, Connecticut, USA
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Juliette Hayer
rSLU, Institutionen för Husdjursgenetik, Uppsala, Sweden
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Hauke Koch
cDepartment of Integrative Biology, University of Texas at Austin, Austin, Texas, USA
sRoyal Botanic Gardens, Kew, Richmond, Surrey, United Kingdom
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Sarah Kocher
tDepartment of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge , Massachusetts , USA
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Vincent G. Martinson
uDepartment of Biology, University of Rochester, Rochester, New York, USA
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Nancy Moran
cDepartment of Integrative Biology, University of Texas at Austin, Austin, Texas, USA
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Monica Munoz-Torres
vEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley , California , USA
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Irene Newton
wDepartment of Biology, Indiana University, Bloomington, Indiana, USA
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Robert J. Paxton
kInstitute for Biology, Martin Luther University Halle-Wittenberg, Halle, Germany
lGerman Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
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Eli Powell
cDepartment of Integrative Biology, University of Texas at Austin, Austin, Texas, USA
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Ben M. Sadd
xSchool of Biological Sciences, Illinois State University, Normal, Illinois, USA
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Paul Schmid-Hempel
yETHZ Institut für Integrative Biologie, Zurich, Switzerland
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Regula Schmid-Hempel
yETHZ Institut für Integrative Biologie, Zurich, Switzerland
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Se Jin Song
zUniversity of Colorado at Boulder, Boulder, Colorado, USA
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Ryan S. Schwarz
mUSDA, ARS Bee Research Laboratory, Beltsville, Maryland, USA
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Dennis vanEngelsdorp
aaDepartment of Entomology, University of Maryland, College Park, Maryland, USA
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Benjamin Dainat
abAgroscope, Swiss Bee Research Centre, Bern, Switzerland
acBee Health Extension Service, Apiservice, Bern , Switzerland
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Gregory B. Hurst
Oak Ridge National Laboratory
Roles: Invited Editor
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R. John Collier
Harvard Medical School
Roles: Editor
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DOI: 10.1128/mBio.02164-15
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    FIG 1 

    A resource and analysis platform for bee microbiome studies. Large amounts of sequence data, metadata, and methods are being generated by different research groups around the globe. A centralized platform is needed to systematically archive such information, to make it available to other researchers in the field, to allow cross-study analyses, and to standardize approaches. The bee microbiome platform will enable more detailed analyses of available data to formulate novel hypotheses about bee health and microbiome evolution.

Tables

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  • TABLE 1 

    Outstanding questions in bee microbiome research

    Field of knowledgeResearch question
    Bee health
        1.How do different microbes impact bee health?
            a.    Nutritional versus defensive symbioses?
            b.    Host range and fitness effects of pathogens?
        2.Which combinations of microbes are most detrimental or beneficial?
        3.Do microbes in wild and managed bee populations influence health in similar ways?
        4.How do environmental factors influence host-microbiome interactions?
        5.How do the interactions among microbiome members modulate the impact of individual members, to the benefit or cost to the host?
    Evolution and ecology
        1.What are the functions of the different microbes in the bee gut?
        2.Which factors drive the composition and evolution of the bee microbiome?
        3.How does the social/solitary lifestyle of bees influence microbiome evolution?
        4.How has domestication changed the bee microbiome?
  • TABLE 2 

    Major challenges for bee microbiome studies

    Area of studyQuestions and considerations
    1. Defining bee healthWhat are the best measures of fitness at the individual and colony levels? In social insects, fitness experiments with individual bees may not reflect the fitness of a colony.
    2. Microbiome compositionHow do distinct microbes interact to affect hosts? Microbes likely influence one another’s effect on the host. Coinfections pose a challenge for disentangling individual roles, and certain experiments may need to be conducted in microbiome-free hosts.
    3. Host geneticsBees are genetically diverse, which may affect microbiome-host interactions. Can the influence of genetic differences among hosts be controlled for?
    4. Environmental factorsThese are likely to contribute to microbiome composition and function. How can such environmental factors be reliably measured and tested?
    5. Physiological variablesThe physiology and development of bees can differ substantially according to season, age, housing, and nutrition. Do these differences influence microbiome relationships?
    6. Microbiome quantificationDifferent diagnostic tools (quantitative and qualitative) exist to study microbiome compositions. How comparable are these tools?
    7. Wild pollinatorsFor the majority of the ~20,000 wild bee species, the microbiome composition and functions are unknown. Systematic and standardized sampling approaches are needed.
    8. Data accessibilitySystematic archiving of large sequencing datasets with accompanying metadata information is crucial so that cross-study analyses can be conducted.
  • TABLE 3 

    Practical steps for advancements

    Challenge and step
    1. Many microbes are important to bee biology, but often an experiment focuses on only one type. Simultaneous screening for 16S rRNA genes, 18S rRNA genes, and viruses is needed to yield a more comprehensive picture of the microbiome.
    2. If simultaneous screening as proposed in step 1 is not feasible, archiving aliquots of DNA/RNA/whole samples will facilitate future identification of the other microbes.
    3. Quantitative PCR of total individual (i.e., per bee) microbial loads will help with the interpretation of relative compositional data, as typically acquired by amplicon sequencing.
    4. Proper metadata are needed for interpretation and comparison of results. As much information as possible should be recorded and made accessible for an experiment.
    5. Standardized experimental bee lines should be established to control for host genetic differences between laboratories.
    6. Standardization of protocols, such as the methods of isolation of host, bacterial, and viral DNA/RNA, is necessary for cross-study analysis.
    7. Sampling and sequencing environmental sources, such as flowers and nest components, will help to understand the spread and transmission of bee microbes.
    8. Bee microbiome researchers should be engaged to actively participate in the bee microbiome project and to help establish this necessary and important community service.

Supplemental Material

  • Figures
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  • Additional Files
  • Table S1 

    Comprehensive overview of Apis bee diseases, including known hosts and known effects on hosts. Table S1, XLSX file, 0.02 MB.

    Copyright © 2016 Engel et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Table S2 

    Comprehensive overview of Apis bee microbes. Table S2, XLSX file, 0.01 MB.

    Copyright © 2016 Engel et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Table S3 

    Comprehensive overview of non-Apis bee microorganisms. Table S3, XLSX file, 0.02 MB.

    Copyright © 2016 Engel et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Text S1 

    Literature support for the Apis bee diseases. Download Text S1, DOCX file, 0.02 MB.

    Copyright © 2016 Engel et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Text S2 

    Literature support for the Apis bee microbes. Download Text S2, PDF file, 0.1 MB.

    Copyright © 2016 Engel et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Text S3 

    Literature support for the non-Apis bee microorganisms. Download Text S3, DOCX file, 0.02 MB.

    Copyright © 2016 Engel et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

Additional Files

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    Supplementary Data

    • Text s1, DOCX - Text s1, DOCX
    • Text s2, PDF - Text s2, PDF
    • Text s3, DOCX - Text s3, DOCX
    • Table st1, XLSX - Table st1, XLSX
    • Table st2, XLSX - Table st2, XLSX
    • Table st3, XLSX - Table st3, XLSX
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The Bee Microbiome: Impact on Bee Health and Model for Evolution and Ecology of Host-Microbe Interactions
Philipp Engel, Waldan K. Kwong, Quinn McFrederick, Kirk E. Anderson, Seth Michael Barribeau, James Angus Chandler, R. Scott Cornman, Jacques Dainat, Joachim R. de Miranda, Vincent Doublet, Olivier Emery, Jay D. Evans, Laurent Farinelli, Michelle L. Flenniken, Fredrik Granberg, Juris A. Grasis, Laurent Gauthier, Juliette Hayer, Hauke Koch, Sarah Kocher, Vincent G. Martinson, Nancy Moran, Monica Munoz-Torres, Irene Newton, Robert J. Paxton, Eli Powell, Ben M. Sadd, Paul Schmid-Hempel, Regula Schmid-Hempel, Se Jin Song, Ryan S. Schwarz, Dennis vanEngelsdorp, Benjamin Dainat
mBio Apr 2016, 7 (2) e02164-15; DOI: 10.1128/mBio.02164-15

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The Bee Microbiome: Impact on Bee Health and Model for Evolution and Ecology of Host-Microbe Interactions
Philipp Engel, Waldan K. Kwong, Quinn McFrederick, Kirk E. Anderson, Seth Michael Barribeau, James Angus Chandler, R. Scott Cornman, Jacques Dainat, Joachim R. de Miranda, Vincent Doublet, Olivier Emery, Jay D. Evans, Laurent Farinelli, Michelle L. Flenniken, Fredrik Granberg, Juris A. Grasis, Laurent Gauthier, Juliette Hayer, Hauke Koch, Sarah Kocher, Vincent G. Martinson, Nancy Moran, Monica Munoz-Torres, Irene Newton, Robert J. Paxton, Eli Powell, Ben M. Sadd, Paul Schmid-Hempel, Regula Schmid-Hempel, Se Jin Song, Ryan S. Schwarz, Dennis vanEngelsdorp, Benjamin Dainat
mBio Apr 2016, 7 (2) e02164-15; DOI: 10.1128/mBio.02164-15
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  • Top
  • Article
    • ABSTRACT
    • INTRODUCTION
    • MICROBIOME AS A COMPONENT OF BEE HEALTH
    • THE BEE MICROBIOME AS AN EVOLUTIONARY MODEL FOR SYMBIOSIS
    • PERSPECTIVE: CHALLENGES AND NOVEL APPROACHES
    • CONCLUSIONS
    • ACKNOWLEDGMENTS
    • REFERENCES
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