Cell Host & Microbe
Volume 29, Issue 10, 13 October 2021, Pages 1545-1557.e4
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Article
Symbiont-regulated serotonin biosynthesis modulates tick feeding activity

https://doi.org/10.1016/j.chom.2021.08.011Get rights and content
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Highlights

  • A reduction in the abundance of the symbiont Coxiella impairs blood intake in ticks

  • Diminished Coxiella abundance reduces serotonin biosynthesis within the tick

  • Serotonin is pivotal in regulating tick feeding activity

  • Coxiella-derived chorismate, a tryptophan precursor, promotes serotonin biosynthesis

Summary

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.

Keywords

Coxiella
tick
serotonin
feeding activity
Haemaphysalis longicornis

Data and code availability

The published article includes all datasets generated or analyzed during this study.

The raw RNA-Seq sequencing data were uploaded to the National Center for Biotechnology Information’s Sequence Read Archive (SRA: PRJNA693137).

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