Unity in defence: honeybee workers exhibit conserved molecular responses to diverse pathogens View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2017-03-02

AUTHORS

Vincent Doublet, Yvonne Poeschl, Andreas Gogol-Döring, Cédric Alaux, Desiderato Annoscia, Christian Aurori, Seth M. Barribeau, Oscar C. Bedoya-Reina, Mark J. F. Brown, James C. Bull, Michelle L. Flenniken, David A. Galbraith, Elke Genersch, Sebastian Gisder, Ivo Grosse, Holly L. Holt, Dan Hultmark, H. Michael G. Lattorff, Yves Le Conte, Fabio Manfredini, Dino P. McMahon, Robin F. A. Moritz, Francesco Nazzi, Elina L. Niño, Katja Nowick, Ronald P. van Rij, Robert J. Paxton, Christina M. Grozinger

ABSTRACT

BackgroundOrganisms typically face infection by diverse pathogens, and hosts are thought to have developed specific responses to each type of pathogen they encounter. The advent of transcriptomics now makes it possible to test this hypothesis and compare host gene expression responses to multiple pathogens at a genome-wide scale. Here, we performed a meta-analysis of multiple published and new transcriptomes using a newly developed bioinformatics approach that filters genes based on their expression profile across datasets. Thereby, we identified common and unique molecular responses of a model host species, the honey bee (Apis mellifera), to its major pathogens and parasites: the Microsporidia Nosema apis and Nosema ceranae, RNA viruses, and the ectoparasitic mite Varroa destructor, which transmits viruses.ResultsWe identified a common suite of genes and conserved molecular pathways that respond to all investigated pathogens, a result that suggests a commonality in response mechanisms to diverse pathogens. We found that genes differentially expressed after infection exhibit a higher evolutionary rate than non-differentially expressed genes. Using our new bioinformatics approach, we unveiled additional pathogen-specific responses of honey bees; we found that apoptosis appeared to be an important response following microsporidian infection, while genes from the immune signalling pathways, Toll and Imd, were differentially expressed after Varroa/virus infection. Finally, we applied our bioinformatics approach and generated a gene co-expression network to identify highly connected (hub) genes that may represent important mediators and regulators of anti-pathogen responses.ConclusionsOur meta-analysis generated a comprehensive overview of the host metabolic and other biological processes that mediate interactions between insects and their pathogens. We identified key host genes and pathways that respond to phylogenetically diverse pathogens, representing an important source for future functional studies as well as offering new routes to identify or generate pathogen resilient honey bee stocks. The statistical and bioinformatics approaches that were developed for this study are broadly applicable to synthesize information across transcriptomic datasets. These approaches will likely have utility in addressing a variety of biological questions. More... »

PAGES

207

References to SciGraph publications

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  • Journal

    TITLE

    BMC Genomics

    ISSUE

    1

    VOLUME

    18

    Author Affiliations

  • Centre for Ecology and Conservation, University of Exeter, Penryn, UK
  • Institute of Computer Science, Martin Luther University Halle-Wittenberg, Halle (Saale), Germany
  • Technische Hochschule Mittelhessen, Gießen, Germany
  • INRA, UR 406 Abeilles et Environnement, Avignon, France
  • Dipartimento di Scienze AgroAlimentari, Ambientali e Animali, Università degli Studi di Udine, Udine, Italy
  • Institute of Life Sciences, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, Romania
  • Department of Biology, East Carolina University, Greenville, NC, USA
  • Present address: MRC Functional Genomics Unit, Department of Physiology, Anatomy and Genetics, University of Oxford, South Parks Road, Oxford, UK
  • School of Biological Sciences, Royal Holloway University of London, Egham, Surrey, UK
  • Department of Biosciences, Swansea University, Swansea, UK
  • Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, MT, USA
  • Department of Entomology, Center for Pollinator Research, Pennsylvania State University, State College, PA, USA
  • Department of Microbiology and Epizootics, Freie Universität Berlin, Berlin, Germany
  • Department of Molecular Microbiology and Bee Diseases, Institute for Bee Research, Hohen Neuendorf, Germany
  • Department of Fisheries, Wildlife, and Conservation Biology, The Monarch Joint Venture, University of Minnesota, St. Paul, MN, USA
  • Department of Molecular Biology, Umeå University, Umeå, Sweden
  • Present address: International Centre of Insect Physiology and Ecology (icipe), Environmental Health Theme, Nairobi, Kenya
  • Department for Materials and Environment, BAM Federal Institute for Materials Research and Testing, Berlin, Germany
  • Institute for Biology, Martin Luther University Halle-Wittenberg, Halle (Saale), Germany
  • Department of Entomology and Nematology, University of California, Davis, CA, USA
  • Paul-Flechsig-Institute for Brain Research, University of Leipzig, Leipzig, Germany
  • Department of Medical Microbiology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands
  • School of Biological Sciences, Queen’s University Belfast, Belfast, UK
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1186/s12864-017-3597-6

    DOI

    http://dx.doi.org/10.1186/s12864-017-3597-6

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1084250065

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/28249569


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    539 grid-institutes:grid.9647.c schema:alternateName Paul-Flechsig-Institute for Brain Research, University of Leipzig, Leipzig, Germany
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    542 Paul-Flechsig-Institute for Brain Research, University of Leipzig, Leipzig, Germany
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