Microbial ecology of the hive and pollination landscape: Bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera)

Authors: Anderson, Kirk; Sheehan, Timothy; Mott, Brendon; Maes, Patrick; Snyder, Lucy; Schwan, Melissa; WALTON, ALEXANDER - Former ARS Employee; JONES, BERYL - Former ARS Employee; Corby-Harris, Vanessa

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/11/2013
Publication Date: 12/17/2013
Citation: Anderson, K.E., Sheehan, T.H., Mott, B.M., Maes, P.W., Snyder, L.A., Schwan, M.R., Walton, A., Jones, B., Corby-Harris, V.L. 2013. Microbial ecology of the hive and pollination landscape: Bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera). PLoS One. 8(12):e83125. DOI: 10.1371/journal.pone.0083125.

Interpretive Summary: Nearly all multi-cellular animals are host to beneficial or benign bacteria in their gut lumen that are either inherited from previous generations or acquired from the environment. While the core bacteria of the honey bee gut is becoming evident, the influence of the pollination environment on honey bee-associated microbial populations is virtually unexplored. Recent findings from social and solitary bees suggest that bacteria living with plants may play a major role in pollinator fitness. Here we use multiple approaches to investigate bacteria from different segments of the honey bee (Apis mellifera) gut, incoming pollen, and stored pollen. Our results reveal that many non-core bacteria prevalent in stored pollen and the honey bee gut niche are typically associated with the above ground plant surface, pollen or floral nectar. One pollination environment revealed an abundance of Coliform related bacteria, including many possible pathogens and food spoilage organisms, while another contained potentially beneficial bacteria including Lactobacillus kunkeei, Fructobacillus spp. and many different groups of Actinobacteria. We suggest that a subset of bacteria associated with plants and floral nectar can provide benefits throughout the acidic and sugar-rich hive environment. Contributions of plant-associated bacteria to colony health may include general hygiene, fungal and pathogen inhibition and beebread preservation. Changes in the pollination environment, due to both typical environmental variation and human influence could affect honey bee colony health by directly or indirectly altering the evolution, abundance or survival of potentially beneficial or pathogenic bacteria on the plant surface, flower or honey bee food stores. 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 colony food storage and disease susceptibility.

Technical Abstract: Nearly all eukaryotes are host to beneficial or benign bacteria in their gut lumen that are either vertically inherited or acquired from the environment. While the core bacteria of the honey bee gut is becoming evident, the influence of the pollination environment on honey bee-associated microbial populations is virtually unexplored. Recent findings from social and solitary bees suggest that bacteria living with plants may play a major role in pollinator fitness. Here we use culturing, 16S cloning and sequencing, phylogenetic inference and bioinformatics to investigate bacteria from different segments of the honey bee (Apis mellifera) gut, incoming pollen, and stored pollen. Our results reveal that many non-core bacteria prevalent in stored pollen and the honey bee gut niche are typically associated with the plant phylosphere, pollen or floral nectar. One pollination environment revealed an abundance of Enterobacteriaceae, including many possible pathogens and food spoilage organisms, while another contained potentially beneficial bacteria including Lactobacillus kunkeei, Fructobacillus spp. and many different groups of Actinobacteria. We suggest that a subset of bacteria associated with phylosphere and floral nectar can serve as facultative mutualists throughout the acidic and sugar-rich hive environment. Contributions of plant-associated bacteria to colony health may include general hygiene, fungal and pathogen inhibition and beebread preservation. Changes in the pollination environment, due to both typical environmental variation and human influence could affect honey bee colony health by directly or indirectly altering the evolution, abundance or survival of potentially beneficial or pathogenic bacteria in the phylosphere, flower or honey bee food stores. 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 colony food storage and disease susceptibility.