Chronic Nosema ceranae infection inflicts comprehensive and persistent immunosuppression and accelerated lipid loss in host Apis mellifera honey bees

Authors: LI, WENFENG - Zhejiang University; Chen, Yanping - Judy; Cook, Steven

Submitted to: International Journal for Parasitology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/7/2017
Publication Date: 2/13/2018
Citation: Li, W., Chen, Y., Cook, S.C. 2018. Chronic Nosema ceranae infection inflicts comprehensive and persistent immunosuppression and accelerated lipid loss in host Apis mellifera honey bees. International Journal for Parasitology. 48:433-444. https://doi.org/10.1016/j.ijpara.2017.11.004.
DOI: https://doi.org/10.1016/j.ijpara.2017.11.004

Interpretive Summary: Nosema ceranae is an intracellular fungal (microsporidian) gut pathogen that infects Apis mellifera honey bees. N. ceranae causes significant harm to infected honey bees by suppressing aspects of their host's immune system, and are believed to cause their hosts energetic stress due to the fact that Nosema lack functional mitochondria (power houses of cells). Nosema disease is associated with precocious (early) foraging of young adult ‘nurse’ bees, and this can be a leading cause of honey bee colony collapse, a phenomenon which continues to threaten U.S. food security. In this study, we expanded the investigation of host immunosuppression and showed that Nosema comprehensively and persistently suppresses the two major innate immune system responses, Imd and Toll. In addition, we expanded the investigation of host energetic stress and demonstrated that infection decreased lipid content, and increased metabolic rate and activity of infected honey bees. We learned that lipid, and not sugar metabolism may be the source of energetic stress experienced by infected honey bees. This finding is important because lipid content of young adult bees is an important factor determining the timing when ‘nurse’ bees transition into foragers; foragers contain lower lipid content than nurses. Our work identifies a possible mechanism explaining why nurse bees infected with Nosema forage earlier than those that are uninfected.

Technical Abstract: Nosema ceranae is an intracellular microsporidian parasite of the Asian honey bee Apis cerana and the European honey bee A. mellifera. Until recently, A. mellifera honey bees were naïve to N. ceranae infection. Symptoms of Nosemosis, or Nosema disease, in the infected hosts include immunosuppression, damage to gut epithelium, nutrient and energetic stress, and precocious foraging and reduced longevity of infected bees. Linkages remain unclear between immunosuppression, the symptoms of nutrient and energetic stress, and precocious foraging behavior of hosts. To clarify physiological connections, we inoculated newly-emerged A. mellifera adult workers with N. ceranae spores, and over 21 days post inoculation (21 dpi), gauged infection intensity and quantified expression of genes representing two innate immune pathways, Toll, and Imd. Additionally, we measured host’s whole-body protein, lipids, carbohydrate, and quantified respirometric and activity levels. Results show sustained suppression of genes of both humorally regulated immune response pathways after 6 dpi. At 7 dpi, an elevated protein of infected bees may reflect synthesis of antimicrobial peptides from an initial immune response, but the lack of protein gain compared to uninfected bees at 14 dpi may represent low de novo protein synthesis. Carbohydrate data do not indicate hosts experience severe metabolic stress related to this nutrient. At 14 dpi infected honey bees show high respirometric and activity levels, and corresponding lipid loss, suggesting lipids may be favored over carbohydrates as fuel for increased metabolic demands from infection. Accelerated lipid loss during nurse honey bee behavioral development can have cascading effects on downstream physiology that may lead to precocious foraging, which is a major factor driving colony collapse.