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Title: Systemic spread and propagation of a plant pathogenic virus in European honey bees, Apis mellifera

item LI, JILIAN - Chinese Academy Of Agricultural Sciences
item CORNMAN, ROBERT - Us Geological Survey (USGS)
item Evans, Jay
item Pettis, Jeffery
item Zhao, Yan
item Murphy, Charles
item Hammond, John
item PENG, WENJUN - Chinese Academy Of Agricultural Sciences
item WU, JIE - Chinese Academy Of Agricultural Sciences
item BONCRISTIANI, HUMBERTO - University Of North Carolina
item ZHOU, LIANG - Emory University, School Of Medicine
item Chen, Yanping - Judy

Submitted to: mBio
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/13/2013
Publication Date: 1/21/2014
Citation: Li, J., Cornman, R., Evans, J.D., Pettis, J.S., Zhao, Y., Murphy, C.F., Hammond, J., Peng, W., Wu, J., Boncristiani, H., Zhou, L., Chen, Y. 2014. Systemic spread and propagation of a plant pathogenic virus in European honey bees, Apis mellifera. mBio. 5(1):e00898-13. DOI: 10.1128/mBio.00898-13.

Interpretive Summary: Pathogen host shifts represent a major source of new infectious diseases. Honey bees are exposed to diverse plant viruses when foraging and when consuming food derived from pollen and nectar, but they are not known to be hosts for their replication. Here we provide evidence that a pollen-borne plant virus also replicates in honey bees. The virus was found to systemically invade and replicate in different body parts. In addition, the virus was detected inside the body of Varroa mites, common ectoparasites that consume bee hemolymph, suggesting that Varroa mites may play a role in facilitating the spread of the virus in bee colonies. This study represents the first evidence that honey bees exposed to virus-contaminated pollen could also be infected and raises awareness of potential risks of new viral disease emergence due to host shift events. About 5% of known plant viruses are pollen transmitted which are potential sources of future host-jumping viruses. The findings from this study showcase the need for increased surveillance for potential host-jumping events as an integrated part of insect pollinator management programs.

Technical Abstract: Emerging and reemerging diseases that result from pathogen host shifting are a threat to the health of humans and their domesticates. RNA viruses are ubiquitous and have extremely high mutation rates and thus represent a significant source of these infectious diseases. In the present study, we showed that a plant pathogenic RNA virus, Tobacco ringspot virus (TRSV) could replicate and produce virions in European honey bees, Apis mellifera. The infection was found throughout the entire body but titers were highest in the nervous system, suggesting neurotrophism in honey bees. Unlike many bee viruses that are ingested and then disseminate from the midgut to other tissues via the hemolymph, TRSV appears to invade through another route, possibly involving neural, tracheal, or muscle tissues. TRSV was also detected in ectoparasitic mites that feed on bee hemolymph (Varroa destructor), but however, in those instances the virus was restricted to the gastric caecum of Varroa mites. This suggests that Varroa destructor may facilitate the spread of TRSV in bee colonies but does not experience systemic invasion. A phyologenetic analysis of capisid gene sequences revealed that TRSV isolates from honey bees, bee bread and Varroa mites clustered together, forming a monophyletic clade. The tree topology indicated that the TRSVs from arthropod hosts shared a common ancestor with those from plant hosts, and subsequently evolved as a distinct lineage after trans-kingdom host alteration. It would be intriguing to learn whether the amino acid substitutions that occurred in deduced capsid protein sequences of honeybee TRSV isolates are associated with host adaptation and play a role in tissue tropism of the virus. This study represents a unique example of viruses with host ranges spanning both plant and animal kingdoms.