Research Article: Honey bee (Apis mellifera) exposomes and dysregulated metabolic pathways associated with Nosema ceranae infection

Date Published: March 7, 2019

Publisher: Public Library of Science

Author(s): Robert L. Broadrup, Christopher Mayack, Sassicaia J. Schick, Elizabeth J. Eppley, Helen K. White, Anthony Macherone, Eric Jan.


Honey bee (Apis mellifera) health has been severely impacted by multiple environmental stressors including parasitic infection, pesticide exposure, and poor nutrition. The decline in bee health is therefore a complex multifactorial problem which requires a holistic investigative approach. Within the exposome paradigm, the combined exposure to the environment, drugs, food, and individuals’ internal biochemistry affects health in positive and negative ways. In the context of the exposome, honey bee hive infection with parasites such as Nosema ceranae is also a form of environmental exposure. In this study, we hypothesized that exposure to xenobiotic pesticides and other environmental chemicals increases susceptibility to N. ceranae infection upon incidental exposure to the parasite. We further queried whether these exposures could be linked to changes in conserved metabolic biological pathways. From 30 hives sampled across 10 sites, a total of 2,352 chemical features were found via gas chromatography-time of flight mass spectrometry (GC-TOF) in extracts of honey bees collected from each hive. Of these, 20 pesticides were identified and annotated, and found to be significantly associated with N. ceranae infection. We further determined that infected hives were linked to a greater number of xenobiotic exposures, and the relative concentration of the exposures were not linked to the presence of a N. ceranae infection. In the exposome profiles of the bees, we also found chemicals inherent to known biological metabolic pathways of Apis mellifera and identified 9 dysregulated pathways. These findings have led us to posit that for hives exposed to similar chemicals, those that incur multiple, simultaneous xenobiotic stressors have a greater incidence of infection with N. ceranae. Mechanistically, our results suggests the overwhelming nature of these exposures negatively affects the biological functioning of the bee, and could explain how the decline in bee populations is associated with pesticide exposures.

Partial Text

Bees are essential to maintaining biodiversity, and their services as crop pollinators cannot be overstated[1–5]. Over the past decade global honey bee populations have been severely reduced by various environmental stressors including but not limited to: poor nutrition, losses in foraging habitats, infectious exposures to viruses and parasites, and exposures to pesticides and other persistent chemicals[6–9]. Each of these individual stressors represents environmental exposures that adversely affect bee health at the colony level. Moreover, these environmental exposures may interact with one another and synergistically effect the overall health of the hive[10–12]. One study indicated that the interaction between viral infections and the parasitic mite, Varroa destructor, is a primary cause of honey bee colony mortality[13]. In another study, the probability of infection by the fungus, Nosema spp., has also been found to be substantially increased when bees are concomitantly exposed to fungicides[14, 15]. Finally, Nosema spp. infection coupled with exposure to the neonicotinoid pesticide imidacloprid has been observed to weaken the ability of honey bees to sterilize the colony and brood food, rendering the hive more susceptible to pathogens[11]. These studies suggest that there is a complex relationship between environmental stressors and hive survivability, implying that a more holistic approach is needed to determine how potential causal factors interact to result in bee health decline.




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