O2-Sensing Neurons Control CO2 Response in C. elegans

Abstract

Sensory behaviors are often flexible, allowing animals to generate context-appropriate responses to changing environmental conditions. To investigate the neural basis of behavioral flexibility, we examined the regulation of carbon dioxide (CO2) response in the nematode Caenorhabditis elegans. CO2 is a critical sensory cue for many animals, mediating responses to food, conspecifics, predators, and hosts (Buehlmann et al., 2012; Chaisson and Hallem, 2012; Scott, 2011). In C. elegans, CO2 response is regulated by the polymorphic neuropeptide receptor NPR-1: animals with the N2 allele of npr-1 avoid CO2, while animals with the Hawaiian (HW) allele or an npr-1 loss-of-function (lf) mutation appear virtually insensitive to CO2 (Hallem and Sternberg, 2008; McGrath et al., 2009). Here we show that ablating the oxygen (O2)-sensing URX neurons in npr-1(lf) mutants restores CO2 avoidance, suggesting that NPR-1 enables CO2 avoidance by inhibiting URX neurons. URX was previously shown to be activated by increases in ambient O2 (Busch et al., 2012; Persson et al., 2009; Zimmer et al., 2009). We find that in npr-1(lf) mutants, O2-induced activation of URX inhibits CO2 avoidance. Moreover, both HW and npr-1(lf) animals avoid CO2 under low O2 conditions, when URX is inactive. Our results demonstrate that CO2 response is determined by the activity of O2-sensing neurons, and suggest that O2-dependent regulation of CO2 avoidance is likely to be an ecologically relevant mechanism by which nematodes navigate gas gradients.

A Single Set of Interneurons Drives Opposite Behaviors in C. elegans

“…We previously showed that the BAG sensory neurons detect CO 2 and are required for CO 2 avoidance [12, 15, 20]. We therefore examined the role of BAG in mediating CO 2 attraction.…”

A Chemoreceptor That Detects Molecular Carbon Dioxide

“…Another mechanism by which CO 2 sensing might be regulated by the metabolic state of the animal is a functional connection between neurons that monitor internal oxygen concentration and the BAG neurons. CO 2 avoidance behavior is modulated by hypoxia (22), and oxygen-sensing neurons functionally inhibit the CO 2 avoidance behavior that is driven by BAG neurons (43).…”

Memory of recent oxygen experience switches pheromone valence in Caenorhabditis elegans

“…Animals escaping 21% O 2 will thus often encounter high CO 2 , creating conflicting drives that could be ecologically significant. Previous work showed that natural C. elegans isolates immediately suppress CO 2 avoidance when O 2 levels approach 21%, due to increased tonic signaling from URX O 2 sensors (37)(38)(39)(40) lawn of bacteria kept at 7% O 2 . After halting briefly, animals acclimated to 7% O 2 became persistently aroused at 3% CO 2 (Fig.…”