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

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      a , , b , c , d , e , f , g , h , i , j , k , l , a , m , n , o , p , q , a , b , r , c , s , t , u , c , v , w , k , l , c , x , y , y , z , m , aa , ab , ac ,
      mBio
      American Society for Microbiology

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          ABSTRACT

          As pollinators, bees are cornerstones for terrestrial ecosystem stability and key components in agricultural productivity. All animals, including bees, are associated with a diverse community of microbes, commonly referred to as the microbiome. The bee microbiome is likely to be a crucial factor affecting host health. However, with the exception of a few pathogens, the impacts of most members of the bee microbiome on host health are poorly understood. Further, the evolutionary and ecological forces that shape and change the microbiome are unclear. Here, we discuss recent progress in our understanding of the bee microbiome, and we present challenges associated with its investigation. We conclude that global coordination of research efforts is needed to fully understand the complex and highly dynamic nature of the interplay between the bee microbiome, its host, and the environment. High-throughput sequencing technologies are ideal for exploring complex biological systems, including host-microbe interactions. To maximize their value and to improve assessment of the factors affecting bee health, sequence data should be archived, curated, and analyzed in ways that promote the synthesis of different studies. To this end, the BeeBiome consortium aims to develop an online database which would provide reference sequences, archive metadata, and host analytical resources. The goal would be to support applied and fundamental research on bees and their associated microbes and to provide a collaborative framework for sharing primary data from different research programs, thus furthering our understanding of the bee microbiome and its impact on pollinator health.

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          Most cited references56

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          Immune pathways and defence mechanisms in honey bees Apis mellifera

          Social insects are able to mount both group-level and individual defences against pathogens. Here we focus on individual defences, by presenting a genome-wide analysis of immunity in a social insect, the honey bee Apis mellifera. We present honey bee models for each of four signalling pathways associated with immunity, identifying plausible orthologues for nearly all predicted pathway members. When compared to the sequenced Drosophila and Anopheles genomes, honey bees possess roughly one-third as many genes in 17 gene families implicated in insect immunity. We suggest that an implied reduction in immune flexibility in bees reflects either the strength of social barriers to disease, or a tendency for bees to be attacked by a limited set of highly coevolved pathogens.
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            Influence of Pollen Nutrition on Honey Bee Health: Do Pollen Quality and Diversity Matter?

            Honey bee colonies are highly dependent upon the availability of floral resources from which they get the nutrients (notably pollen) necessary to their development and survival. However, foraging areas are currently affected by the intensification of agriculture and landscape alteration. Bees are therefore confronted to disparities in time and space of floral resource abundance, type and diversity, which might provide inadequate nutrition and endanger colonies. The beneficial influence of pollen availability on bee health is well-established but whether quality and diversity of pollen diets can modify bee health remains largely unknown. We therefore tested the influence of pollen diet quality (different monofloral pollens) and diversity (polyfloral pollen diet) on the physiology of young nurse bees, which have a distinct nutritional physiology (e.g. hypopharyngeal gland development and vitellogenin level), and on the tolerance to the microsporidian parasite Nosema ceranae by measuring bee survival and the activity of different enzymes potentially involved in bee health and defense response (glutathione-S-transferase (detoxification), phenoloxidase (immunity) and alkaline phosphatase (metabolism)). We found that both nurse bee physiology and the tolerance to the parasite were affected by pollen quality. Pollen diet diversity had no effect on the nurse bee physiology and the survival of healthy bees. However, when parasitized, bees fed with the polyfloral blend lived longer than bees fed with monofloral pollens, excepted for the protein-richest monofloral pollen. Furthermore, the survival was positively correlated to alkaline phosphatase activity in healthy bees and to phenoloxydase activities in infected bees. Our results support the idea that both the quality and diversity (in a specific context) of pollen can shape bee physiology and might help to better understand the influence of agriculture and land-use intensification on bee nutrition and health.
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              Nutrition and health in honey bees

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                Author and article information

                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                26 April 2016
                Mar-Apr 2016
                : 7
                : 2
                : e02164-15
                Affiliations
                [a ]Department of Fundamental Microbiology, University of Lausanne, Lausanne, Switzerland
                [b ]Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, USA
                [c ]Department of Integrative Biology, University of Texas at Austin, Austin, Texas, USA
                [d ]Department of Entomology, University of California, Riverside, California, USA
                [e ]USDA, Carl Hayden Bee Research Center, Tucson, Arizona, USA
                [f ]Department of Biology, East Carolina University, Greenville, North Carolina, USA
                [g ]Department of Microbiology, California Academy of Sciences, San Francisco, California, USA
                [h ]U.S. Geological Survey, Fort Collins Science Center, Fort Collins, Colorado, USA
                [i ]Bioinformatics Infrastructure for Life Sciences (BILS), Linköpings Universitet Victoria Westling, Linköping, Sweden, and Department of Medical Biochemistry and Microbiology Uppsala University, Uppsala, Sweden
                [j ]Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden
                [k ]Institute for Biology, Martin Luther University Halle-Wittenberg, Halle, Germany
                [l ]German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
                [m ]USDA, ARS Bee Research Laboratory, Beltsville, Maryland, USA
                [n ]Fasteris SA, Plan -les-Ouates, Switzerland
                [o ]Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, Montana, USA
                [p ]SLU, BVF, Virologi, Uppsala, Sweden
                [q ]Department of Biology, North Life Sciences, San Diego State University, San Diego, California, USA
                [r ]SLU, Institutionen för Husdjursgenetik, Uppsala, Sweden
                [s ]Royal Botanic Gardens, Kew, Richmond, Surrey, United Kingdom
                [t ]Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge , Massachusetts , USA
                [u ]Department of Biology, University of Rochester, Rochester, New York, USA
                [v ]Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley , California , USA
                [w ]Department of Biology, Indiana University, Bloomington, Indiana, USA
                [x ]School of Biological Sciences, Illinois State University, Normal, Illinois, USA
                [y ]ETHZ Institut für Integrative Biologie, Zurich, Switzerland
                [z ]University of Colorado at Boulder, Boulder, Colorado, USA
                [aa ]Department of Entomology, University of Maryland, College Park, Maryland, USA
                [ab ]Agroscope, Swiss Bee Research Centre, Bern, Switzerland
                [ac ]Bee Health Extension Service, Apiservice, Bern , Switzerland
                Author notes
                Address correspondence to Philipp Engel, philipp.engel@ 123456unil.ch , or Benjamin Dainat, benjamin.dainat@ 123456agroscope.admin.ch .
                [*]

                Present address: James Angus Chandler, Department of Molecular and Cell Biology, University of California, Berkeley, California, USA

                Invited Editor Gregory B. Hurst, Oak Ridge National Laboratory Editor R. John Collier, Harvard Medical School

                Author information
                http://orcid.org/0000-0002-0335-0386
                http://orcid.org/0000-0003-0750-5709
                http://orcid.org/0000-0002-1740-7136
                Article
                mBio02164-15
                10.1128/mBio.02164-15
                4850275
                27118586
                aaa62503-ec98-4410-b4a0-1f0394cddbfe
                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.

                History
                Page count
                supplementary-material: 7, Figures: 1, Tables: 3, Equations: 0, References: 100, Pages: 9, Words: 8835
                Funding
                This manuscript arose from the discussions by the Bee Microbiome consortium at the National Evolutionary Synthesis Center (NESCent) workshop "BeeBiome:Omic approaches for understanding bee-microbe relationships" held in Durham, NC, USA from 20 to 24th October 2014. The workshop was supported by the National Evolutionary Synthesis Center (NESCent), grant NSF #EF-0905606 to B.D., P.E., J.R.M., J.D.E., and L.G.
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                March/April 2016

                Life sciences
                Life sciences

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