Single and mixed-species trypanosome and microsporidia infections elicit distinct, ephemeral cellular and humoral immune responses in honey bees

Authors: Schwarz, Ryan; Evans, Jay

Submitted to: Developmental and Comparative Immunology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/21/2013
Publication Date: 5/20/2013
Citation: Schwarz, R.S., Evans, J.D. 2013. Single and mixed-species trypanosome and microsporidia infections elicit distinct, ephemeral cellular and humoral immune responses in honey bees. Developmental and Comparative Immunology. 40:300-310.

Interpretive Summary: Impacts of parasitic infections on their hosts may be driven by genetic and environmental factors, as well as the presence of additional microbial populations within the host. Though all microbial infections have a metabolic cost on their host, the net impact may vary from harmful to beneficial. Such variation may depend in part on combinations of co-infecting microbes that impact one another and their host in unique ways. The effects of two common microbes that infect honey bees were investigated: the trypanosome Crithidia mellificae and/or the microsporidian Nosema ceranae. Highly sensitive and specific molecular methods were used to monitor honey bee immune responses to these common parasites. Distinct immune responses toward each parasite were identified. Bees infected with both parasites had altered immune responses that were distinct from either parasite individually. This work shows that honey bees respond uniquely to distinct types of parasites and that honey bee immune responses are altered when they are infected with more than one parasite at a time.

Technical Abstract: Frequently encountered parasite species impart strong selective pressures on host immune system evolution and are more apt to concurrently infect the same host, yet molecular impacts in light of this are often overlooked. We have contrasted immune responses in honey bees to two common eukaryotic endoparasites by establishing single and mixed-species infections using the long-associated parasite Crithidia mellificae and the emergent parasite Nosema ceranae. Quantitative polymerase chain reaction was used to screen host immune gene expression at 9 time points post inoculation. Systemic responses in abdomens during early stages of parasite establishment revealed conserved receptor (Down syndrome cell adhesion molecule, Dscam and nimrod C1, nimC1), signaling (MyD88 and Imd) and antimicrobial peptide (AMP) effector (Defensin 2) responses. Late, established infections were distinct with a refined 2 AMP response to C. mellificae that contrasted starkly with a 5 AMP response to N. ceranae. Mixed species infections induced a moderate 3 AMPs. Transcription in gut tissues highlighted important local roles for Dscam toward both parasites and Imd signaling toward N. ceranae. At both systemic and local levels Dscam, MyD88 and Imd transcription was consistently correlated based on clustering analysis. Significant gene suppression occurred in two cases from midgut-ileum tissue: Dscam was lowered during mixed infections compared to N. ceranae infections and both C. mellificae and mixed infections had reduced nimC1 transcription compared to uninfected controls. We show that honey bees rapidly mount complex immune responses to both Nosema and Crithidia that are dynamic over time and that mixed-species infections significantly alter local and systemic immune gene transcription.