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

Andrew Jonathan Bretscher,Eiji Kodama-Namba,Karl Emanuel Busch,Robin Joseph Murphy,Zoltan Soltesz,Patrick Laurent,Mario De Bono

doi:10.1016/j.neuron.2011.02.023

Andrew Jonathan Bretscher, Eiji Kodama-Namba + Show 5 more

Open Access

https://doi.org/10.1016/j.neuron.2011.02.023

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Journal: Neuron	Publication Date: Mar 1, 2011
Citations: 171	License type: cc-by

Affiliation: MRC Laboratory of Molecular Biology

Abstract

SummaryHomeostatic 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.

Highlights

As the major by-product of oxidative metabolism, CO2 is ubiquitous in nature
But not all, of the Ca2+ responses to CO2 depend on a cGMP-gated ion channel
Multiple Sensory Neurons Mediate C. elegans Avoidance of CO2 When placed in a 5%-0% CO2 gradient, C. elegans migrate away from high CO2 (Figures 1A and 1B) (Bretscher et al, 2008)

Summary

Introduction

As the major by-product of oxidative metabolism, CO2 is ubiquitous in nature. CO2 comprises only $0.038% of Earth’s atmosphere, it can accumulate to higher levels in environments with high respiration rates (Lahiri and Forster, 2003). Mice can smell environmental CO2 concentrations as low as 0.066% CO2 using specialized olfactory neurons that express carbonic anhydrase II (Hu et al, 2007). CO2 levels of 10% or more elicit an innate fear response in which animals freeze and avoid open spaces (Ziemann et al, 2009). This response requires activation of the acid-sensing ion channel ASIC-1A in cells of the amygdala (Ziemann et al, 2009). High concentrations of inhaled CO2 modulate wakefulness by stimulating midbrain neurons (Williams et al, 2007; Richerson, 2004; Buchanan and Richerson, 2010)

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Discussion

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