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

Abstract

Carbon dioxide (CO 2 ) gradients are ubiquitous and provide animals with information about their environment, such as the potential presence of prey or predators. The nematode Caenorhabditis elegans avoids elevated CO 2 , and previous work identified three neuron pairs called "BAG," "AFD," and "ASE" that respond to CO 2 stimuli. Using in vivo Ca 2+ imaging and behavioral analysis, we show that C. elegans can detect CO 2 independently of these sensory pathways. Many of the C. elegans sensory neurons we examined, including the AWC olfactory neurons, the ASJ and ASK gustatory neurons, and the ASH and ADL nociceptors, respond to a rise in CO 2 with a rise in Ca 2+ . In contrast, glial sheath cells harboring the sensory endings of C. elegans' major chemosensory neurons exhibit strong and sustained decreases in Ca 2+ in response to high CO 2 . Some of these CO 2 responses appear to be cell intrinsic. Worms therefore may couple detection of CO 2 to that of other cues at the earliest stages of sensory processing. We show that C. elegans persistently suppresses oviposition at high CO 2 . Hermaphrodite-specific neurons (HSNs), the executive neurons driving egg-laying, are tonically inhibited when CO 2 is elevated. CO 2 modulates the egg-laying system partly through the AWC olfactory neurons: High CO 2 tonically activates AWC by a cGMP-dependent mechanism, and AWC output inhibits the HSNs. Our work shows that CO 2 is a more complex sensory cue for C. elegans than previously thought, both in terms of behavior and neural circuitry.neural circuit | behavioral choice | olfactory system | oviposition | glia M ost living matter creates temporal or spatial gradients of carbon dioxide (CO 2 ). Animals across phylogeny use such gradients to help detect food, conspecifics, or predators (1, 2). 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.CO 2 crosses membranes readily and dissolves to generate CO 2 (aq), H + , and HCO 3 − . Many proteins whose activity is modified by CO 2 or its solvation products have been identified. pH changes can modulate G protein-coupled receptors (7), Ca 2+ -activated K + channels (8), inwardly rectifying K + channels (9), two pore domain K + channels (10), transient receptor potential (TRP) channels (11, 12), acid-sensing ion channels (ASICs) (13,14), and Pyk2 and ErbB1/2 kinases (15). HCO 3 − modulates soluble adenylate cyclase (16) and transmembrane guanylate cyclases (17); and CO 2 (aq) has been proposed to regulate transmembrane guanylate cyclases (18) and connexin 26 (19) directly. Cells expressing any of these proteins potentially could transduce changes in CO 2 /H + , raising the question: Do animals use a few specific sensory channe...

Mechanisms of host seeking by parasitic nematodes

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Memory of recent oxygen experience switches pheromone valence in Caenorhabditis elegans

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