The innate immune and systemic response in honey bees to a bacterial pathogen, Paenibacillus larvae

Queenie Wt Chan,Stephen F Pernal,Leonard J Foster,Andony P Melathopoulos

doi:10.1186/1471-2164-10-387

Queenie Wt Chan, Stephen F Pernal + Show 2 more

Open Access

https://doi.org/10.1186/1471-2164-10-387

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Abstract

BackgroundThere is a major paradox in our understanding of honey bee immunity: the high population density in a bee colony implies a high rate of disease transmission among individuals, yet bees are predicted to express only two-thirds as many immunity genes as solitary insects, e.g., mosquito or fruit fly. This suggests that the immune response in bees is subdued in favor of social immunity, yet some specific immune factors are up-regulated in response to infection. To explore the response to infection more broadly, we employ mass spectrometry-based proteomics in a quantitative analysis of honey bee larvae infected with the bacterium Paenibacillus larvae. Newly-eclosed bee larvae, in the second stage of their life cycle, are susceptible to this infection, but become progressively more resistant with age. We used this host-pathogen system to probe not only the role of the immune system in responding to a highly evolved infection, but also what other mechanisms might be employed in response to infection.ResultsUsing quantitative proteomics, we compared the hemolymph (insect blood) of five-day old healthy and infected honey bee larvae and found a strong up-regulation of some metabolic enzymes and chaperones, while royal jelly (food) and energy storage proteins were down-regulated. We also observed increased levels of the immune factors prophenoloxidase (proPO), lysozyme and the antimicrobial peptide hymenoptaecin. Furthermore, mass spectrometry evidence suggests that healthy larvae have significant levels of catalytically inactive proPO in the hemolymph that is proteolytically activated upon infection. Phenoloxidase (PO) enzyme activity was undetectable in one or two-day-old larvae and increased dramatically thereafter, paralleling very closely the age-related ability of larvae to resist infection.ConclusionWe propose a model for the host response to infection where energy stores and metabolic enzymes are regulated in concert with direct defensive measures, such as the massive enhancement of PO activity.

Highlights

There is a major paradox in our understanding of honey bee immunity: the high population density in a bee colony implies a high rate of disease transmission among individuals, yet bees are predicted to express only two-thirds as many immunity genes as solitary insects, e.g., mosquito or fruit fly
Evans et al found no changes in defensin gene expression in larvae fed P. larvae spores and, paradoxically, that abaecin gene expression was greatest in newly eclosed larvae [8,9], the most susceptible stage
Different strains of P. larvae produce equivalent outcomes In order to test the response of worker larvae to P. larvae infection, we spray-inoculated a small section of comb containing one-day-old worker larvae with either (A) a homogenate of scale from natural infections of P. larvae (PL-Scale) or (B) a laboratory-cultured strain of P. larvae (NRRL B-3650, PL-Lab)

Summary

Introduction

There is a major paradox in our understanding of honey bee immunity: the high population density in a bee colony implies a high rate of disease transmission among individuals, yet bees are predicted to express only two-thirds as many immunity genes as solitary insects, e.g., mosquito or fruit fly. Newlyeclosed bee larvae, in the second stage of their life cycle, are susceptible to this infection, but become progressively more resistant with age We used this host-pathogen system to probe the role of the immune system in responding to a highly evolved infection, and what other mechanisms might be employed in response to infection. Bees are only susceptible to P. larvae during the first 48 h following eclosion (egg hatching), in their first and second instar developmental stages It remains unclear why larvae acquire immunity against P. larvae after the third instar, whereas the ingestion of merely 10 spores can cause systemic infection and death in the previous instars [2]. We explore the response of this system to a physiologically relevant infection in a natural setting

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