Abstract

Animals from diverse phyla possess neurons that are activated by the product of aerobic respiration, CO2. It has long been thought that such neurons primarily detect the CO2 metabolites protons and bicarbonate. We have determined the chemical tuning of isolated CO2 chemosensory BAG neurons of the nematode Caenorhabditis elegans. We show that BAG neurons are principally tuned to detect molecular CO2, although they can be activated by acid stimuli. One component of the BAG transduction pathway, the receptor-type guanylate cyclase GCY-9, suffices to confer cellular sensitivity to both molecular CO2 and acid, indicating that it is a bifunctional chemoreceptor. We speculate that in other animals, receptors similarly capable of detecting molecular CO2 might mediate effects of CO2 on neural circuits and behavior.

Highlights

  • C. elegans BAG neurons respond to environmental CO2

  • We observed that the receptor-type guanylate cyclase GCY-9, which is an essential component of the sensory transduction apparatus in BAG neurons and is likely to function as part of a receptor complex [24], is enriched in the terminus of the BAG cell neurite (Fig. 1, B and C)

  • The remarkable tuning of C. elegans BAG neurons to molecular CO2 distinguishes them from previously characterized CO2 chemoreceptor neurons

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Summary

A Chemoreceptor That Detects Molecular Carbon Dioxide*

Received for publication, September 9, 2013, and in revised form, October 21, 2013 Published, JBC Papers in Press, November 15, 2013, DOI 10.1074/jbc.M113.517367 Ewan St. John Smith‡§1, Luis Martinez-Velazquez‡, and Niels Ringstad‡2 From the ‡Skirball Institute of Biomolecular Medicine, Molecular Neurobiology Program and Department of Cell Biology, New York University Medical Center, New York, New York 10016 and the §Department of Pharmacology, University of Cambridge, Cambridge, CB2 1PD, United Kingdom

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