Co-option of neurotransmitter signaling for inter-organismal communication in C. elegans

Christopher D. Chute, Elizabeth M. DiLoreto, Ying K. Zhang, Douglas K. Reilly, Diego Rayes, Veronica L. Coyle, Hee June Choi, Mark J. Alkema, Frank C. Schroeder and Jagan Srinivasan ()
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Christopher D. Chute: Worcester Polytechnic Institute
Elizabeth M. DiLoreto: Worcester Polytechnic Institute
Ying K. Zhang: Cornell University
Douglas K. Reilly: Worcester Polytechnic Institute
Diego Rayes: University of Massachusetts Medical School
Veronica L. Coyle: Worcester Polytechnic Institute
Hee June Choi: Worcester Polytechnic Institute
Mark J. Alkema: University of Massachusetts Medical School
Frank C. Schroeder: Cornell University
Jagan Srinivasan: Worcester Polytechnic Institute

Nature Communications, 2019, vol. 10, issue 1, 1-13

Abstract: Abstract Biogenic amine neurotransmitters play a central role in metazoan biology, and both their chemical structures and cognate receptors are evolutionarily conserved. Their primary roles are in cell-to-cell signaling, as biogenic amines are not normally recruited for communication between separate individuals. Here, we show that in the nematode C. elegans, a neurotransmitter-sensing G protein-coupled receptor, TYRA-2, is required for avoidance responses to osas#9, an ascaroside pheromone that incorporates the neurotransmitter, octopamine. Neuronal ablation, cell-specific genetic rescue, and calcium imaging show that tyra-2 expression in the nociceptive neuron, ASH, is necessary and sufficient to induce osas#9 avoidance. Ectopic expression in the AWA neuron, which is generally associated with attractive responses, reverses the response to osas#9, resulting in attraction instead of avoidance behavior, confirming that TYRA-2 partakes in the sensing of osas#9. The TYRA-2/osas#9 signaling system represents an inter-organismal communication channel that evolved via co-option of a neurotransmitter and its cognate receptor.

Date: 2019
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DOI: 10.1038/s41467-019-11240-7

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