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PLoS Pathog. 2009 June; 5(6): e1000466.
Published online 2009 June 5. doi: 10.1371/journal.ppat.1000466.
PMCID: PMC2685015
Genomic Analyses of the Microsporidian Nosema ceranae, an Emergent Pathogen of Honey Bees
R. Scott Cornman,1 Yan Ping Chen,1 Michael C. Schatz,2 Craig Street,3 Yan Zhao,4 Brian Desany,5 Michael Egholm,5 Stephen Hutchison,5 Jeffery S. Pettis,1 W. Ian Lipkin,3 and Jay D. Evans1*
1USDA-ARS Bee Research Lab, Beltsville, Maryland, United States of America
2Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland, United States of America
3Center for Infection and Immunity, Mailman School of Public Health, Columbia University, New York, New York, United States of America
4USDA-ARS Molecular Plant Pathology Laboratory, Beltsville, Maryland, United States of America
5454 Life Sciences/Roche Applied Sciences, Branford, Connecticut, United States of America
Alex Andrianopoulos, Editor
University of Melbourne, Australia
* E-mail: Jay.evans/at/ars.usda.gov
Conceived and designed the experiments: YPC JSP WIL JDE. Performed the experiments: YPC ME SH WIL. Analyzed the data: RSC MCS CS YZ BD JDE. Contributed reagents/materials/analysis tools: RSC YPC MCS JSP WIL JDE. Wrote the paper: RSC YPC JDE.
Received March 10, 2009; Accepted May 5, 2009.
Abstract
Recent steep declines in honey bee health have severely impacted the beekeeping industry, presenting new risks for agricultural commodities that depend on insect pollination. Honey bee declines could reflect increased pressures from parasites and pathogens. The incidence of the microsporidian pathogen Nosema ceranae has increased significantly in the past decade. Here we present a draft assembly (7.86 MB) of the N. ceranae genome derived from pyrosequence data, including initial gene models and genomic comparisons with other members of this highly derived fungal lineage. N. ceranae has a strongly AT-biased genome (74% A+T) and a diversity of repetitive elements, complicating the assembly. Of 2,614 predicted protein-coding sequences, we conservatively estimate that 1,366 have homologs in the microsporidian Encephalitozoon cuniculi, the most closely related published genome sequence. We identify genes conserved among microsporidia that lack clear homology outside this group, which are of special interest as potential virulence factors in this group of obligate parasites. A substantial fraction of the diminutive N. ceranae proteome consists of novel and transposable-element proteins. For a majority of well-supported gene models, a conserved sense-strand motif can be found within 15 bases upstream of the start codon; a previously uncharacterized version of this motif is also present in E. cuniculi. These comparisons provide insight into the architecture, regulation, and evolution of microsporidian genomes, and will drive investigations into honey bee–Nosema interactions.
Author Summary
Honey bee colonies are in decline in many parts of the world, in part due to pressures from a diverse assemblage of parasites and pathogens. The range and prevalence of the microsporidian pathogen Nosema ceranae has increased significantly in the past decade. Here we describe the N. ceranae genome, presenting genome traits, gene models and regulatory motifs. N. ceranae has an extremely reduced and AT-biased genome, yet one with substantial numbers of repetitive elements. We identify novel genes that appear to be conserved among microsporidia but undetected outside this phylum, which are of special interest as potential virulence factors for these obligate pathogens. A previously unrecognized motif is found upstream of many start codons and likely plays a role in gene regulation across the microsporidia. These and other comparisons provide insight into the architecture, regulation, and evolution of microsporidian genomes, and provide the first genetic tools for understanding how this pathogen interacts with honey bee hosts.