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Iridovirus and Microsporidian Linked to Honey Bee Colony Decline

http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0013181

Jerry J. Bromenshenk1,7*, Colin B. Henderson2,7, Charles H. Wick3, Michael F. Stanford3, Alan W. Zulich3, Rabih E. Jabbour4, Samir V. Deshpande5,13, Patrick E. McCubbin6, Robert A. Seccomb7, Phillip M. Welch7, Trevor Williams8, David R. Firth9, Evan Skowronski3, Margaret M. Lehmann10, Shan L. Bilimoria11,14, Joanna Gress12, Kevin W. Wanner12, Robert A. Cramer Jr10
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

Abstract Top
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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