Symbiont-regulated serotonin biosynthesis modulates tick feeding activity

Ticks are obligate hematophagous arthropods. Blood feeding ensures that ticks obtain nutrients essential for their survival, development, and reproduction while providing routes for pathogen transmission. However, the effectors that determine tick feeding activities remain poorly understood. Here, we demonstrate that reduced abundance of the symbiont Coxiella (CHI) in Haemaphysalis longicornis decreases blood intake. Providing tetracycline-treated ticks with the CHI-derived tryptophan precursor chorismate, tryptophan, or 5-hydroxytryptamine (5-HT; serotonin) restores the feeding defect. Mechanistically, CHI-derived chorismate increases tick 5-HT biosynthesis by stimulating the expression of aromatic amino acid decarboxylase (AAAD), which catalyzes the decarboxylation of 5-hydroxytryptophan (5-HTP) to 5-HT. The increased level of 5-HT in the synganglion and midgut promotes tick feeding. Inhibition of CHI chorismate biosynthesis by treating the colonized tick with the herbicide glyphosate suppresses blood-feeding behavior. Taken together, our results demonstrate an important function of the endosymbiont Coxiella in the regulation of tick 5-HT biosynthesis and feeding.