Microbial Ecology of the Hive and Pollination Landscape: Bacterial Associates from Floral Nectar, the Alimentary Tract and Stored Food of Honey Bees (Apis mellifera)

Nearly all eukaryotes are host to beneficial or benign bacteria in their gut lumen, either vertically inherited, or acquired from the environment. While bacteria core to the honey bee gut are becoming evident, the influence of the hive and pollination environment on honey bee microbial health is lar...

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Veröffentlicht in:PloS one 2013-12, Vol.8 (12), p.e83125-e83125
Hauptverfasser: Anderson, Kirk E, Sheehan, Timothy H, Mott, Brendon M, Maes, Patrick, Snyder, Lucy, Schwan, Melissa R, Walton, Alexander, Jones, Beryl M, Corby-Harris, Vanessa, Gerardo, Nicole M
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container_issue 12
container_start_page e83125
container_title PloS one
container_volume 8
creator Anderson, Kirk E
Sheehan, Timothy H
Mott, Brendon M
Maes, Patrick
Snyder, Lucy
Schwan, Melissa R
Walton, Alexander
Jones, Beryl M
Corby-Harris, Vanessa
Gerardo, Nicole M
description Nearly all eukaryotes are host to beneficial or benign bacteria in their gut lumen, either vertically inherited, or acquired from the environment. While bacteria core to the honey bee gut are becoming evident, the influence of the hive and pollination environment on honey bee microbial health is largely unexplored. Here we compare bacteria from floral nectar in the immediate pollination environment, different segments of the honey bee (Apis mellifera) alimentary tract, and food stored in the hive (honey and packed pollen or “beebread”). We used cultivation and sequencing to explore bacterial communities in all sample types, coupled with culture-independent analysis of beebread. We compare our results from the alimentary tract with both culture-dependent and culture-independent analyses from previous studies. Culturing the foregut (crop), midgut and hindgut with standard media produced many identical or highly similar 16S rDNA sequences found with 16S rDNA clone libraries and next generation sequencing of 16S rDNA amplicons. Despite extensive culturing with identical media, our results do not support the core crop bacterial community hypothesized by recent studies. We cultured a wide variety of bacterial strains from 6 of 7 phylogenetic groups considered core to the honey bee hindgut. Our results reveal that many bacteria prevalent in beebread and the crop are also found in floral nectar, suggesting frequent horizontal transmission. From beebread we uncovered a variety of bacterial phylotypes, including many possible pathogens and food spoilage organisms, and potentially beneficial bacteria including Lactobacillus kunkeei , Acetobacteraceae and many different groups of Actinobacteria. Contributions of these bacteria to colony health may include general hygiene, fungal and pathogen inhibition and beebread preservation. Our results are important for understanding the contribution to pollinator health of both environmentally vectored and core microbiota, and the identification of factors that may affect bacterial detection and transmission, colony food storage and disease susceptibility.
doi_str_mv 10.1371/journal.pone.0083125
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Our results are important for understanding the contribution to pollinator health of both environmentally vectored and core microbiota, and the identification of factors that may affect bacterial detection and transmission, colony food storage and disease susceptibility.</description><subject>Acetobacteraceae</subject><subject>Acromyrmex octospinosus</subject><subject>Actinobacteria</subject><subject>alimentary tract</subject><subject>Analysis</subject><subject>Animals</subject><subject>Antibiotics</subject><subject>Apis mellifera</subject><subject>Bacteria</subject><subject>Bacteria - isolation &amp; purification</subject><subject>bacterial communities</subject><subject>Bacteriological Techniques</subject><subject>Bees</subject><subject>Bees - microbiology</subject><subject>Bees - physiology</subject><subject>Colonies</subject><subject>Crop diseases</subject><subject>Crops</subject><subject>Cultivation</subject><subject>Culture</subject><subject>Culture media</subject><subject>Digestive tract</subject><subject>disease resistance</subject><subject>Disease susceptibility</subject><subject>Disease transmission</subject><subject>DNA, Bacterial - genetics</subject><subject>Ecology</subject><subject>Endophytes - isolation &amp; purification</subject><subject>Eukaryotes</subject><subject>eukaryotic cells</subject><subject>European honeybee</subject><subject>Flowers</subject><subject>food pathogens</subject><subject>Food spoilage</subject><subject>Food storage</subject><subject>Foregut</subject><subject>Fungi</subject><subject>Gastrointestinal tract</subject><subject>Gastrointestinal Tract - microbiology</subject><subject>Grocery stores</subject><subject>Health</subject><subject>high-throughput nucleotide sequencing</subject><subject>Hindgut</subject><subject>Honey</subject><subject>Honey - microbiology</subject><subject>honey bees</subject><subject>Hygiene</subject><subject>Insects</subject><subject>intestinal microorganisms</subject><subject>Lactobacillus kunkeei</subject><subject>microbial detection</subject><subject>Microbiota</subject><subject>Microbiota (Symbiotic organisms)</subject><subject>Microorganisms</subject><subject>Midgut</subject><subject>Nectar</subject><subject>nucleotide sequences</subject><subject>Nutrition</subject><subject>Pathogens</subject><subject>Phylogeny</subject><subject>phylotype</subject><subject>Plant Nectar</subject><subject>Plant reproduction</subject><subject>Pollen</subject><subject>Pollination</subject><subject>Pollinators</subject><subject>Preservation</subject><subject>Probiotics</subject><subject>propolis</subject><subject>rDNA</subject><subject>ribosomal DNA</subject><subject>RNA, Ribosomal, 16S - 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microbiology</topic><topic>honey bees</topic><topic>Hygiene</topic><topic>Insects</topic><topic>intestinal microorganisms</topic><topic>Lactobacillus kunkeei</topic><topic>microbial detection</topic><topic>Microbiota</topic><topic>Microbiota (Symbiotic organisms)</topic><topic>Microorganisms</topic><topic>Midgut</topic><topic>Nectar</topic><topic>nucleotide sequences</topic><topic>Nutrition</topic><topic>Pathogens</topic><topic>Phylogeny</topic><topic>phylotype</topic><topic>Plant Nectar</topic><topic>Plant reproduction</topic><topic>Pollen</topic><topic>Pollination</topic><topic>Pollinators</topic><topic>Preservation</topic><topic>Probiotics</topic><topic>propolis</topic><topic>rDNA</topic><topic>ribosomal DNA</topic><topic>RNA, Ribosomal, 16S - genetics</topic><topic>rRNA 16S</topic><topic>Spoilage</topic><topic>Symbiosis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Anderson, Kirk E</creatorcontrib><creatorcontrib>Sheehan, Timothy H</creatorcontrib><creatorcontrib>Mott, Brendon M</creatorcontrib><creatorcontrib>Maes, Patrick</creatorcontrib><creatorcontrib>Snyder, Lucy</creatorcontrib><creatorcontrib>Schwan, Melissa R</creatorcontrib><creatorcontrib>Walton, Alexander</creatorcontrib><creatorcontrib>Jones, Beryl M</creatorcontrib><creatorcontrib>Corby-Harris, Vanessa</creatorcontrib><creatorcontrib>Gerardo, Nicole M</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing &amp; Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological &amp; Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>ProQuest Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science &amp; Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies &amp; Aerospace Collection</collection><collection>Agricultural &amp; Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Anderson, Kirk E</au><au>Sheehan, Timothy H</au><au>Mott, Brendon M</au><au>Maes, Patrick</au><au>Snyder, Lucy</au><au>Schwan, Melissa R</au><au>Walton, Alexander</au><au>Jones, Beryl M</au><au>Corby-Harris, Vanessa</au><au>Gerardo, Nicole M</au><au>Gerardo, Nicole M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Microbial Ecology of the Hive and Pollination Landscape: Bacterial Associates from Floral Nectar, the Alimentary Tract and Stored Food of Honey Bees (Apis mellifera)</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-12-17</date><risdate>2013</risdate><volume>8</volume><issue>12</issue><spage>e83125</spage><epage>e83125</epage><pages>e83125-e83125</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Nearly all eukaryotes are host to beneficial or benign bacteria in their gut lumen, either vertically inherited, or acquired from the environment. While bacteria core to the honey bee gut are becoming evident, the influence of the hive and pollination environment on honey bee microbial health is largely unexplored. Here we compare bacteria from floral nectar in the immediate pollination environment, different segments of the honey bee (Apis mellifera) alimentary tract, and food stored in the hive (honey and packed pollen or “beebread”). We used cultivation and sequencing to explore bacterial communities in all sample types, coupled with culture-independent analysis of beebread. We compare our results from the alimentary tract with both culture-dependent and culture-independent analyses from previous studies. Culturing the foregut (crop), midgut and hindgut with standard media produced many identical or highly similar 16S rDNA sequences found with 16S rDNA clone libraries and next generation sequencing of 16S rDNA amplicons. Despite extensive culturing with identical media, our results do not support the core crop bacterial community hypothesized by recent studies. We cultured a wide variety of bacterial strains from 6 of 7 phylogenetic groups considered core to the honey bee hindgut. Our results reveal that many bacteria prevalent in beebread and the crop are also found in floral nectar, suggesting frequent horizontal transmission. From beebread we uncovered a variety of bacterial phylotypes, including many possible pathogens and food spoilage organisms, and potentially beneficial bacteria including Lactobacillus kunkeei , Acetobacteraceae and many different groups of Actinobacteria. Contributions of these bacteria to colony health may include general hygiene, fungal and pathogen inhibition and beebread preservation. Our results are important for understanding the contribution to pollinator health of both environmentally vectored and core microbiota, and the identification of factors that may affect bacterial detection and transmission, colony food storage and disease susceptibility.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24358254</pmid><doi>10.1371/journal.pone.0083125</doi><tpages>e83125</tpages><oa>free_for_read</oa></addata></record>
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subjects Acetobacteraceae
Acromyrmex octospinosus
Actinobacteria
alimentary tract
Analysis
Animals
Antibiotics
Apis mellifera
Bacteria
Bacteria - isolation & purification
bacterial communities
Bacteriological Techniques
Bees
Bees - microbiology
Bees - physiology
Colonies
Crop diseases
Crops
Cultivation
Culture
Culture media
Digestive tract
disease resistance
Disease susceptibility
Disease transmission
DNA, Bacterial - genetics
Ecology
Endophytes - isolation & purification
Eukaryotes
eukaryotic cells
European honeybee
Flowers
food pathogens
Food spoilage
Food storage
Foregut
Fungi
Gastrointestinal tract
Gastrointestinal Tract - microbiology
Grocery stores
Health
high-throughput nucleotide sequencing
Hindgut
Honey
Honey - microbiology
honey bees
Hygiene
Insects
intestinal microorganisms
Lactobacillus kunkeei
microbial detection
Microbiota
Microbiota (Symbiotic organisms)
Microorganisms
Midgut
Nectar
nucleotide sequences
Nutrition
Pathogens
Phylogeny
phylotype
Plant Nectar
Plant reproduction
Pollen
Pollination
Pollinators
Preservation
Probiotics
propolis
rDNA
ribosomal DNA
RNA, Ribosomal, 16S - genetics
rRNA 16S
Spoilage
Symbiosis
title Microbial Ecology of the Hive and Pollination Landscape: Bacterial Associates from Floral Nectar, the Alimentary Tract and Stored Food of Honey Bees (Apis mellifera)
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