Chronic parasitization by Nosema microsporidia causes global expression changes in core nutritional, metabolic and behavioral pathways in honey bee workers (Apis mellifera).
BACKGROUND
Chronic infections can profoundly affect the physiology, behavior, fitness and longevity of individuals, and may alter the organization and demography of social groups. Nosema apis and Nosema ceranae are two microsporidian parasites which chronically infect the digestive tract of honey bees (Apis mellifera). These parasites, in addition to other stressors, have been linked to increased mortality of individual workers and colony losses in this key pollinator species. Physiologically, Nosema infection damages midgut tissue, is energetically expensive and alters expression of immune genes in worker honey bees. Infection also accelerates worker transition from nursing to foraging behavior (termed behavioral maturation). Here, using microarrays, we characterized global gene expression patterns in adult worker honey bee midgut and fat body tissue in response to Nosema infection.


RESULTS
Our results indicate that N. apis infection in young workers (1 and 2 days old) disrupts midgut development. At 2 and 7 days post-infection in the fat body tissue, N. apis drives metabolic changes consistent with energetic costs of infection. A final experiment characterizing gene expression in the fat bodies of 14 day old workers parasitized with N. apis and N. ceranae demonstrated that Nosema co-infection specifically alters conserved nutritional, metabolic and hormonal pathways, including the insulin signaling pathway, which is also linked to behavioral maturation in workers. Interestingly, in all experiments, Nosema infection did not appear to significantly regulate overall expression of canonical immune response genes, but infection did alter expression of acute immune response genes identified in a previous study. Comparative analyses suggest that changes in nutritional/metabolic processes precede changes in behavioral maturation and immune processes.


CONCLUSIONS
These genome-wide studies of expression patterns can help us disentangle the direct and indirect effects of chronic infection, and understand the molecular pathways that regulate disease symptoms.
Department of Entomology, Center for Pollinator Research, Center for Chemical Ecology, Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, USA. hlh192@psu.edu.
Holly L
HL
Holt
Katherine A
KA
Aronstein
Christina M
CM
Grozinger
D000818:Animals; D001516:Bees / Q000235:genetics / Q000276:immunology / Q000378:metabolism / Q000382:microbiology*; D001522:Behavior, Animal; D005216:Fat Body / Q000378:metabolism / Q000382:microbiology; D041981:Gastrointestinal Tract / Q000378:metabolism / Q000382:microbiology; D020869:Gene Expression Profiling; D005786:Gene Expression Regulation; D017344:Genes, Insect; D005802:Genes, MHC Class II; D006790:Host-Parasite Interactions; D019476:Insect Proteins / Q000235:genetics / Q000378:metabolism; D008297:Male; D053858:Metabolic Networks and Pathways / Q000235:genetics*; D016818:Nosema / Q000276:immunology / Q000502:physiology*; D020411:Oligonucleotide Array Sequence Analysis; D025341:Principal Component Analysis; D059467:Transcriptome
D019476:Insect Proteins