Temperature, Oxygen, and Salt-Sensing Neurons in C. elegans Are Carbon Dioxide Sensors that Control Avoidance Behavior

Homeostatic control of body fluid CO2 is essential in animals but is poorly understood. C. elegans relies on diffusion for gas exchange and avoids environments with elevated CO2. We show that C. elegans temperature, O2, and salt-sensing neurons are also CO2 sensors mediating CO2 avoidance. AFD therm...

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Bibliographic Details
Published in:Neuron (Cambridge, Mass.) Mass.), 2011-03, Vol.69 (6), p.1099-1113
Main Authors: Bretscher, Andrew Jonathan, Kodama-Namba, Eiji, Busch, Karl Emanuel, Murphy, Robin Joseph, Soltesz, Zoltan, Laurent, Patrick, de Bono, Mario
Format: Article
Language:English
Subjects:
Animals
Behavior, Animal - physiology
Caenorhabditis elegans
Calcium - metabolism
Carbon Dioxide
Homeostasis - physiology
Ion Channel Gating - physiology
Motor Activity - physiology
Oxygen
Sensory Receptor Cells - physiology
Sodium Chloride
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Summary:Homeostatic control of body fluid CO2 is essential in animals but is poorly understood. C. elegans relies on diffusion for gas exchange and avoids environments with elevated CO2. We show that C. elegans temperature, O2, and salt-sensing neurons are also CO2 sensors mediating CO2 avoidance. AFD thermosensors respond to increasing CO2 by a fall and then rise in Ca2+ and show a Ca2+ spike when CO2 decreases. BAG O2 sensors and ASE salt sensors are both activated by CO2 and remain tonically active while high CO2 persists. CO2-evoked Ca2+ responses in AFD and BAG neurons require cGMP-gated ion channels. Atypical soluble guanylate cyclases mediating O2 responses also contribute to BAG CO2 responses. AFD and BAG neurons together stimulate turning when CO2 rises and inhibit turning when CO2 falls. Our results show that C. elegans senses CO2 using functionally diverse sensory neurons acting homeostatically to minimize exposure to elevated CO2. ► The major temperature, O2, and salt-sensing neurons of C. elegans are CO2 sensors ► AFD, BAG, and ASE neurons have unique CO2-response properties ► O2-sensing atypical soluble guanylate cyclases also mediate CO2 neuronal responses ► CO2 sensing involves both transient and persistent neuronal responses
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2011.02.023