A search for protein biomarkers links olfactory signal transduction to social immunity

Abstract

BackgroundThe Western honey bee (Apis mellifera L.) is a critical component of human agriculture through its pollination activities. For years, beekeepers have controlled deadly pathogens such as Paenibacillus larvae, Nosema spp. and Varroa destructor with antibiotics and pesticides but widespread chemical resistance is appearing and most beekeepers would prefer to eliminate or reduce the use of in-hive chemicals. While such treatments are likely to still be needed, an alternate management strategy is to identify and select bees with heritable traits that allow them to resist mites and diseases. Breeding such bees is difficult as the tests involved to identify disease-resistance are complicated, time-consuming, expensive and can misidentify desirable genotypes. Additionally, we do not yet fully understand the mechanisms behind social immunity. Here we have set out to discover the molecular mechanism behind hygienic behavior (HB), a trait known to confer disease resistance in bees.ResultsAfter confirming that HB could be selectively bred for, we correlated measurements of this behavior with protein expression over a period of three years, at two geographically distinct sites, using several hundred bee colonies. By correlating the expression patterns of individual proteins with HB scores, we identified seven putative biomarkers of HB that survived stringent control for multiple hypothesis testing. Intriguingly, these proteins were all involved in semiochemical sensing (odorant binding proteins), nerve signal transmission or signal decay, indicative of the series of events required to respond to an olfactory signal from dead or diseased larvae. We then used recombinant versions of two odorant-binding proteins to identify the classes of ligands that these proteins might be helping bees detect.ConclusionsOur data suggest that neurosensory detection of odors emitted by dead or diseased larvae is the likely mechanism behind a complex and important social immunity behavior that allows bees to co-exist with pathogens.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-014-1193-6) contains supplementary material, which is available to authorized users.

Behavioural, physiological and molecular changes in alloparental caregivers may be responsible for selection response for female reproductive investment in honey bees

“…Our indepth proteome comparison identified 4,728 and 5,154 proteins, representing 2,824 and 3,124 protein groups, in ITB and RJB nurse bee antennae, respectively. The amount of proteins discovered here exceeds previous studies due to technological and procedural advances and significantly improves our understanding of the antennal proteome in general (Guarna et al, ; Hu et al, ). More than 1,800 proteins were specifically detected in either ITB or RJB antennae and more proteins were discovered in the RJB antennae.…”

“…However, the complex phenotype of RJBs seems to involve changes in the sensitivity of the antennae that appear to lower the nurse bees' response threshold to larval pheromones without affecting any larval signalling. Breeding efforts for hygienic honey bees have also increased olfactory sensitivity of the antennae to discriminate diseased from healthy brood (Guarna et al, ), lowering their response thresholds (Masterman et al, ). Together, studies in honey bees support the central role of the insect antenna for behavioural tuning and rapid evolutionary change (Leal, ; Schott et al, ) but we cannot rule out additional differences in the central nervous system.…”

“…The annotation of 21 OBPs, 6 CSPs and 170 ORs has contributed some understanding of the peripheral olfactory processing of honey bees (Foret, Wanner, & Maleszka, ; Robertson & Wanner, ). Some information on central olfactory processing in honey bees exists (Galizia, Sachse, Rappert, & Menzel, ) but most studies of honey bee behavioural variation have implicated the peripheral nervous system (Guarna et al, ; Mondet et al, ; Sánchez‐Gracia, Vieira, & Rozas, ) or endocrine organs (Page, Rueppell, & Amdam, ; Ronai et al, ). Affinity and functional assays have established biological function for few CSPs in honey bees, such as OBP1 binding to queen mandibular pheromone (Danty et al, ) and OR11 as a specific receptor of 9‐oxo‐2‐decenoic acid (Wanner et al, ).…”

The chemical ecology of host-parasite interaction as a target of Varroa destructor control agents

“…Hygienic honey bee colonies uncapped cells that contained dummies impregnated with 26 -28 significantly faster than cells with control dummies (Swanson et al 2009). Similar odors from Varroa -infested brood have not yet been identified, but probably exist as VSH behavior, and Varroa resistant lines show differential expression of genes that are likely involved in chemoreception (Parker et al 2012;Guarna et al 2015).…”

“…It is interesting to note that hygienic worker bees (bred based on the freeze-killed brood removal bioassay) detect and remove diseased larvae apparently by identifying specific odors from diseased brood (Swanson et al 2009). Recent proteomic analyses have revealed that two bee OBPs (16 and 18) are more abundantly expressed in hygienic bee lines than in wild-type lines (Guarna et al 2015). Neurotransmitters, particularly octopamine, also play a role in controlling olfactory processes in insects.…”