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      Iridovirus and Microsporidian Linked to Honey Bee Colony Decline

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          Abstract

          Background

          In 2010 Colony Collapse Disorder (CCD), again devastated honey bee colonies in the USA, indicating that the problem is neither diminishing nor has it been resolved. Many CCD investigations, using sensitive genome-based methods, have found small RNA bee viruses and the microsporidia, Nosema apis and N. ceranae in healthy and collapsing colonies alike with no single pathogen firmly linked to honey bee losses.

          Methodology/Principal Findings

          We used Mass spectrometry-based proteomics (MSP) to identify and quantify thousands of proteins from healthy and collapsing bee colonies. MSP revealed two unreported RNA viruses in North American honey bees, Varroa destructor-1 virus and Kakugo virus, and identified an invertebrate iridescent virus (IIV) ( Iridoviridae) associated with CCD colonies. Prevalence of IIV significantly discriminated among strong, failing, and collapsed colonies. In addition, bees in failing colonies contained not only IIV, but also Nosema. Co-occurrence of these microbes consistently marked CCD in (1) bees from commercial apiaries sampled across the U.S. in 2006–2007, (2) bees sequentially sampled as the disorder progressed in an observation hive colony in 2008, and (3) bees from a recurrence of CCD in Florida in 2009. The pathogen pairing was not observed in samples from colonies with no history of CCD, namely bees from Australia and a large, non-migratory beekeeping business in Montana. Laboratory cage trials with a strain of IIV type 6 and Nosema ceranae confirmed that co-infection with these two pathogens was more lethal to bees than either pathogen alone.

          Conclusions/Significance

          These findings implicate co-infection by IIV and Nosema with honey bee colony decline, giving credence to older research pointing to IIV, interacting with Nosema and mites, as probable cause of bee losses in the USA, Europe, and Asia. We next need to characterize the IIV and Nosema that we detected and develop management practices to reduce honey bee losses.

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          Most cited references 27

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          Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search.

          We present a statistical model to estimate the accuracy of peptide assignments to tandem mass (MS/MS) spectra made by database search applications such as SEQUEST. Employing the expectation maximization algorithm, the analysis learns to distinguish correct from incorrect database search results, computing probabilities that peptide assignments to spectra are correct based upon database search scores and the number of tryptic termini of peptides. Using SEQUEST search results for spectra generated from a sample of known protein components, we demonstrate that the computed probabilities are accurate and have high power to discriminate between correctly and incorrectly assigned peptides. This analysis makes it possible to filter large volumes of MS/MS database search results with predictable false identification error rates and can serve as a common standard by which the results of different research groups are compared.
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            High Levels of Miticides and Agrochemicals in North American Apiaries: Implications for Honey Bee Health

            Background Recent declines in honey bees for crop pollination threaten fruit, nut, vegetable and seed production in the United States. A broad survey of pesticide residues was conducted on samples from migratory and other beekeepers across 23 states, one Canadian province and several agricultural cropping systems during the 2007–08 growing seasons. Methodology/Principal Findings We have used LC/MS-MS and GC/MS to analyze bees and hive matrices for pesticide residues utilizing a modified QuEChERS method. We have found 121 different pesticides and metabolites within 887 wax, pollen, bee and associated hive samples. Almost 60% of the 259 wax and 350 pollen samples contained at least one systemic pesticide, and over 47% had both in-hive acaricides fluvalinate and coumaphos, and chlorothalonil, a widely-used fungicide. In bee pollen were found chlorothalonil at levels up to 99 ppm and the insecticides aldicarb, carbaryl, chlorpyrifos and imidacloprid, fungicides boscalid, captan and myclobutanil, and herbicide pendimethalin at 1 ppm levels. Almost all comb and foundation wax samples (98%) were contaminated with up to 204 and 94 ppm, respectively, of fluvalinate and coumaphos, and lower amounts of amitraz degradates and chlorothalonil, with an average of 6 pesticide detections per sample and a high of 39. There were fewer pesticides found in adults and brood except for those linked with bee kills by permethrin (20 ppm) and fipronil (3.1 ppm). Conclusions/Significance The 98 pesticides and metabolites detected in mixtures up to 214 ppm in bee pollen alone represents a remarkably high level for toxicants in the brood and adult food of this primary pollinator. This represents over half of the maximum individual pesticide incidences ever reported for apiaries. While exposure to many of these neurotoxicants elicits acute and sublethal reductions in honey bee fitness, the effects of these materials in combinations and their direct association with CCD or declining bee health remains to be determined.
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              Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera.

              The most crucial stage in the dynamics of virus infections is the mode of virus transmission. In general, transmission of viruses can occur through two pathways: horizontal and vertical transmission. In horizontal transmission, viruses are transmitted among individuals of the same generation, while vertical transmission occurs from mothers to their offspring. Because of its highly organized social structure and crowded population density, the honey bee colony represents a risky environment for the spread of disease infection. Like other plant and animal viruses, bee viruses use different survival strategies, including utilization of both horizontal and vertical routes, to transmit and maintain levels in a host population. In this review, we explore the current knowledge about the honey bee viruses and transmission routes of bee viruses. In addition, different transmission strategies on the persistence and dynamics of host-pathogen interactions are also discussed.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                6 October 2010
                : 5
                : 10
                Affiliations
                [1 ]Division of Biological Sciences, The University of Montana, Missoula, Montana, United States of America
                [2 ]College of Technology, The University of Montana, Missoula, Montana, United States of America
                [3 ]US Army Edgewood Chemical Biological Center, Aberdeen Proving Ground, Edgewood Area, Maryland, United States of America
                [4 ]Science Applications International Corporation, Abingdon, Maryland, United States of America
                [5 ]Science Technology Corporation, Edgewood, Maryland, United States of America
                [6 ]OptiMetrics, Inc., Abingdon, Maryland, United States of America
                [7 ]Bee Alert Technology, Inc., Missoula, Montana, United States of America
                [8 ]Instituto de Ecologia AC, Xalapa, Veracruz, Mexico
                [9 ]Department of Information Systems and Technology, The University of Montana, Missoula, Montana, United States of America
                [10 ]Department of Veterinary Molecular Biology, Montana State University, Bozeman, Montana, United States of America
                [11 ]Department of Biological Sciences, Texas Tech University, Lubbock, Texas, United States of America
                [12 ]Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, Montana, United States of America
                [13 ]Department of Computer and Information Sciences, Towson University, Towson, Maryland, United States of America
                [14 ]Center for Biotechnology and Genomics, Texas Tech University, Lubbock, Texas, United States of America
                University of California Davis, United States of America
                Author notes

                Conceived and designed the experiments: JJB CBH CHW RAC. Performed the experiments: JJB REJ SVD PEM MML JCG RAC. Analyzed the data: JJB CBH PEM PMW RAC. Contributed reagents/materials/analysis tools: SLB KWW RAC. Wrote the paper: JJB CBH CHW MFS AWZ REJ SVD PEM RAS TW DRF SLB RAC. Coordinated overall research team: JJB. Conducted statistical analyses: CBH. Coordinated Army (ECBC) research: CHW. Directed proteomics research: MFS. Organized Army research contribution: AWZ. Conducted proteomics analysis: REJ SVD. Analyzed results using bioinformatics: REJ SVD. Contributed Information Technology guidance: RAS. Set up and annotated proteomics data base: PMW. Consulted on all aspects of Iridoviruses: TW. Coordinated efforts with US Army: DRF. Guided epidemiology approach: EWS. Directed graduate student research: KWW.

                Article
                10-PONE-RA-18438R1
                10.1371/journal.pone.0013181
                2950847
                20949138
                8f6ee076-1591-4c34-a380-a854ff702a12
                This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
                Page count
                Pages: 11
                Categories
                Research Article
                Biochemistry/Bioinformatics
                Biotechnology/Protein Chemistry and Proteomics
                Ecology/Environmental Microbiology
                Virology/Diagnosis
                Infectious Diseases/Fungal Infections

                Uncategorized

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