Known and novel viruses in Belgian honey bees: yearly differences, spatial clustering, and associations with overwintering loss

Author:

Deboutte Ward1ORCID,De Smet Lina2,Brunain Marleen2,Basler Nikolas1ORCID,De Rycke Riet34,Smets Lena1,de Graaf Dirk C.2,Matthijnssens Jelle1ORCID

Affiliation:

1. KU Leuven–University of Leuven, Department of Microbiology, Immunology and Transplantation, Division of Clinical and Epidemiological Virology, Rega Institute, Leuven, Belgium

2. UGent–Ghent University, Department of Biochemistry and Microbiology, Laboratory of Molecular Entomology and Bee Pathology (L-MEB), Ghent, Belgium

3. VIB Center for Inflammation Research and BioImaging Core, Ghent, Belgium

4. Department of Biomedical Molecular Biology, UGent–Ghent University, Ghent, Belgium

Abstract

ABSTRACT In recent years, managed honey bee colonies have been suffering from an increasing number of biotic and abiotic stressors, resulting in numerous losses of colonies worldwide. A pan-European study, EPILOBEE, estimated the colony loss in Belgium to be 32.4% in 2012 and 14.8% in 2013. In the current study, absolute viral loads of four known honey bee viruses (DWV-A, DWV-B, AmFV, and BMLV) and three novel putative honey bee viruses (Apis orthomyxovirus 1, apthili virus, and apparli virus) were determined in 300 Flemish honey bee samples, and associations with winter survival were determined. This revealed that, in addition to the known influence of DWV-A and DWV-B on colony health, one of the newly described viruses (apthili virus) shows a strong yearly difference and is also associated with winter survival. Furthermore, all scrutinized viruses revealed significant spatial clustering patterns, implying that despite the limited surface area of Flanders, local virus transmission is paramount. The vast majority of samples were positive for at least one of the seven investigated viruses, and up to 20% of samples were positive for at least one of the three novel viruses. One of those three, Apis orthomyxovirus 1, was shown to be a genuine honey bee-infecting virus, able to infect all developmental stages of the honey bee, as well as the Varroa destructor mite. These results shed light on the most prevalent viruses in Belgium and their roles in the winter survival of honey bee colonies. IMPORTANCE The western honey bee ( Apis mellifera ) is a highly effective pollinator of flowering plants, including many crops, which gives honey bees an outstanding importance both ecologically and economically. Alarmingly high annual loss rates of managed honey bee colonies are a growing concern for beekeepers and scientists and have prompted a significant research effort toward bee health. Several detrimental factors have been identified, such as varroa mite infestation and disease from various bacterial and viral agents, but annual differences are often not elucidated. In this study, we utilize the viral metagenomic survey of the EPILOBEE project, a European research program for bee health, to elaborate on the most abundant bee viruses of Flanders. We complement the existing metagenomic data with absolute viral loads and their spatial and temporal distributions. Furthermore, we identify Apis orthomyxovirus 1 as a potentially emerging pathogen, as we find evidence for its active replication honey bees.

Publisher

American Society for Microbiology

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