Abstract:
Insects that transmit many of the world’s deadliest animal diseases, for instance
trypanosomosis, find their suitable hosts and avoid non-preferred hosts mostly through
olfactory cues. The waterbuck repellent blend (WRB) comprising geranylacetone,
guaiacol, pentanoic acid, and d-octalactone derived from waterbuck skin odor is a
repellent to some savannah-adapted tsetse flies and reduces trap catches of riverine
species. However, the cellular and molecular mechanisms associated with detection
and coding of the repellent odors remain to be elucidated. Here, we demonstrated that
WRB inhibited blood feeding in both Glossina pallidipes Austen, 1903 and Glossina
fuscipes fuscipes Newstead, 1910. Using the DREAM (Deorphanization of Receptors
based on Expression Alterations in odorant receptor mRNA levels) technique, combined
with ortholog comparison and molecular docking, we predicted the putative odorant
receptors (ORs) for the WRB in G. f. fuscipes, a non-model insect. We show that
exposure of G. f. fuscipes in vivo to WRB odorant resulted in up- and downregulation
of mRNA transcript of several ORs. The WRB component with strong feeding inhibition
altered mRNA transcript differently as compared to an attractant odor, showing these
two odors of opposing valence already segregate at the cellular and molecular levels.
Furthermore, molecular dynamics simulations demonstrated that the predicted ligand–
OR binding pockets consisted mostly of hydrophobic residues with a few hydrogen
bonds but a stable interaction. Finally, our electrophysiological response showed the
olfactory sensory neurons of G. f. fuscipes tuned to the tsetse repellent components in
different sensitivity and selectivity.