carbon dioxide avoidance behavior is integrated with responses to ambient oxygen and food in Caenorhabditis elegans

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 105; no. 23; pp. 8044 - 8049
• Main Authors: Bretscher, Andrew Jonathan, Busch, Karl Emanuel, de Bono, Mario
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 10.06.2008; National Acad Sciences
• Subjects: Alleles; Anaerobiosis - drug effects; Animals; Avoidance Learning - drug effects; Biological Sciences; Caenorhabditis elegans; Caenorhabditis elegans - drug effects; Caenorhabditis elegans - physiology; Caenorhabditis elegans Proteins - metabolism; Carbon dioxide; Carbon Dioxide - pharmacology; Chemotaxis; Cyclic GMP - metabolism; Feeding Behavior - drug effects; Food; Food availability; Food Deprivation; Genetics; Genotype; Hydrogen-Ion Concentration; Hypoxia; Insulin - metabolism; Ion Channel Gating - drug effects; Motor Activity - drug effects; Nematoda; Nematodes; Neurons; Oxygen; Oxygen - metabolism; Receptors; Receptors, Neuropeptide Y - metabolism; Signal Transduction - drug effects
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.0707607105

Homeostasis of internal carbon dioxide (CO₂) and oxygen (O₂) levels is fundamental to all animals. Here we examine the CO₂ response of the nematode Caenorhabditis elegans. This species inhabits rotting material, which typically has a broad CO₂ concentration range. We show that well fed C. elegans avoid CO₂ levels above 0.5%. Animals can respond to both absolute CO₂ concentrations and changes in CO₂ levels within seconds. Responses to CO₂ do not reflect avoidance of acid pH but appear to define a new sensory response. Sensation of CO₂ is promoted by the cGMP-gated ion channel subunits TAX-2 and TAX-4, but other pathways are also important. Robust CO₂ avoidance in well fed animals requires inhibition of the DAF-16 forkhead transcription factor by the insulin-like receptor DAF-2. Starvation, which activates DAF-16, strongly suppresses CO₂ avoidance. Exposure to hypoxia (<1% O₂) also suppresses CO₂ avoidance via activation of the hypoxia-inducible transcription factor HIF-1. The npr-1 215V allele of the naturally polymorphic neuropeptide receptor npr-1, besides inhibiting avoidance of high ambient O₂ in feeding C. elegans, also promotes avoidance of high CO₂. C. elegans integrates competing O₂ and CO₂ sensory inputs so that one response dominates. Food and allelic variation at NPR-1 regulate which response prevails. Our results suggest that multiple sensory inputs are coordinated by C. elegans to generate different coherent foraging strategies.