Quantitative peptidomics reveal brain peptide signatures of behavior

Abstract

The honey bee genome predicts Ϸ100 peptides from 36 prohormones, but the functions of many of these peptides are unknown. We used differential isotope labeling combined with mass spectrometric analysis to quantify Ϸ50% of known bee brain peptides in the context of foraging, with 8 showing robust and dynamic regulation. Some showed differences in brain abundance as a function of experience; specifically, nectar and pollen collection led to quick changes in abundance. These changes were related to the act of food collection, not ingestion, because foragers bring food back to the hive for storage rather than eating it themselves. Other peptide differences in brain abundance were seen in bees that either flew to a nectar feeder or a pollen feeder, but did not yet collect any food. These differences likely reflect well-known predispositions of some bees to collect either nectar or pollen, but not both. Tachykinin, PBAN, and sNPF were among the peptides with the strongest changes in association with nectar and pollen foraging. These peptides are known to be involved in regulating food intake in solitary insects, suggesting an evolutionary connection between that behavior and social foraging. These results demonstrate that it is now possible to use quantitative peptidomics to help determine which brain peptides are bioactive and to elucidate their function in the regulation of behavior.Apis mellifera ͉ behavioral maturation ͉ foraging ͉ neuropeptides B rain peptides play an important role in orchestrating physiological and behavioral processes in animals by functioning as neurohormones, neuromodulators, and neurotransmitters (1). These cell-cell signaling peptides are produced from their corresponding precursor genes by cleavage at specific sites followed by additional posttranslational modifications, a complex process that can make bioactive peptides difficult to predict (2). The availability of genome sequences has led to a new, high-throughput approach for neuropeptide discovery: algorithms that predict cleavage sites in peptide precursors (3, 4) followed by sequencing from brain samples with mass spectrometry (5-7). Applying this methodology to the honey bee genome, Hummon et al. (6) predicted 36 peptide-encoding genes and confirmed 100 endogenous peptides in the bee brain, numbers similar to what is known for other animals such as the fruit fly (Drosophila melanogaster) and the house mouse (Mus musculus) (7,8).As with other species, however, the physiological and behavioral functions of most (neuro)peptides in the honey bee are unknown (2, 9-11). Until very recently, most brain peptides were discovered one at a time via biochemical techniques, and functional experiments focused on physiological effects (12). Recent advances in peptidomics have greatly accelerated peptide characterization (13-15). However, corresponding high-throughput approaches to discover peptide function have been much less common. A goal of this study was to determine whether combining a recently established quantitative peptidomic method with...

Multiple neuropeptides in the Drosophila antennal lobe suggest complex modulatory circuits

“…Neuropeptides can act as neuromodulators and may affect target cells differentially in different physiological and behavioral contexts. Indeed, neuronal peptide levels in honeybees change dramatically in different behavioral phenotypes and due to altered feeding conditions (Brockmann et al, 2009).…”

Social molecular pathways and the evolution of bee societies

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Parasitic and immune-modulation of flight activity in honey bees tracked with optical counters

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