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

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.

Environmental CO 2 inhibits Caenorhabditis elegans egg-laying by modulating olfactory neurons and evokes widespread changes in neural activity

“…These imaging results were unexpected, especially because previous studies failed to detect CO 2 -evoked Ca 2+ responses in the nociceptive ADL (6) and ASH neurons (5,6). Such discrepancies may reflect differences in stimulus regimes, imaging conditions, Ca 2+ indicators, or transgenic lines used.…”

“…Faster movement was maintained while CO 2 was high (Fig. 1A) (5). When CO 2 dropped from 5 to 0%, N2 animals transiently sped up before gradually settling (Fig.…”

“…A cGMP-gated ion channel subunit encoded by tax-4 sustains CO 2 responses not only in BAG neurons but also in AFD and probably in ASE neurons (5). Like gcy-9 mutants and BAGablated animals, tax-4(p678null) mutants showed severe defects in turning following a 0-5% rise in CO 2 (Fig.…”

“…The ubiquity of CO 2 suggests that the ecologically relevant information it communicates will depend on the dynamics of the CO 2 stimulus and on context. CO 2 -responsive excitable cells have been identified in mammals (3), arthropods (4), and nematodes (5,6). However, the number of CO 2 -responsive neurons that are functional in vivo, how they are embedded in neural circuits, and how they shape behavior is unclear.…”

“…Three neurons that respond robustly to CO 2 have been identified thus far in this animal: BAG neurons that also respond to O 2 , the thermosensory AFD neurons, and the gustatory ASE neurons (5,6). CO 2 responses in BAG neurons are mediated by a receptor-type guanylate cyclase, GCY-9, that signals via a cGMP-gated ion channel encoded by the tax-2 and tax-4 genes (6).…”