Brain Membrane Proteome and Phosphoproteome Reveal Molecular Basis Associating with Nursing and Foraging Behaviors of Honeybee Workers

The
brain is a vital organ in regulating complex social behaviors
of honeybees including learning and memory. Knowledge of how brain
membrane proteins and their phosphorylation underlie the age-related
behavioral polyethism is still lacking. A hitherto age-resolved brain
membrane proteome and phosphoproteome were reported in adult worker
bees from two strains of honeybee (Apis mellifera ligustica): Italian bee (ITB) and Royal Jelly bee (RJB), a line selected from
ITB for increased RJ outputs over four decades. There were 1079 membrane
protein groups identified, and 417 unique phosphosites were located
in 179 membrane protein groups mainly phosphorylated by kinase families
of MAPKs, CDKs, and CK2. Age-resolved dynamics of brain membrane proteome
and phosphoproteome are indicative of their correlation with the neurobiological
requirements during the adult life of honeybee workers. To stimulate
immature brain cell development in newly emerged bees (NEBs), the
enriched functional classes associated with metabolism of carbohydrates,
nucleosides, and lipids by the up-regulated proteins suggest their
enhanced role in driving cell maturity of the brain. In nurse bees
(NBs) and forager bees (FBs), a higher number of membrane proteins
and phosphoproteins were expressed as compared with in the young stages,
and the enriched signal-transduction-related pathways by the up-regulated
proteins suggest their significances in sustaining the intensive information
processing during nursing and foraging activities. Notably, RJB has
shaped unique membrane proteome and phosphoproteome settings to consolidate
nursing and foraging behaviors in response to decades of selection
underpinning the elevated RJ yields. In RJB NBs, the enriched pathways
of phosphatidylinositol signaling and arachidonic acid metabolism
indicate a stronger olfaction sensation in response to larval pheromone
stimulation. In RJB FBs, the enriched pathways related to signal processing
such as SNARE interactions in vesicular transport, wnt signaling,
TGF-beta signaling, and taurine and hypotaurine metabolism suggest
an enhanced nerve sensitivity to prime the stronger tendency to pollen
collection. Our data gain a novel insight into membrane proteome and
phosphoproteome-driven cerebral regulation of honeybee behaviors,
which is potentially useful for further neurobiological investigation
in both honeybees and other social insects.