Abstract
Specialized oxygen-sensing cells in the nervous system generate rapid behavioural responses to oxygen. We show here that the nematode Caenorhabditis elegans exhibits a strong behavioural preference for 5-12% oxygen, avoiding higher and lower oxygen levels. 3',5'-cyclic guanosine monophosphate (cGMP) is a common second messenger in sensory transduction and is implicated in oxygen sensation. Avoidance of high oxygen levels by C. elegans requires the sensory cGMP-gated channel tax-2/tax-4 and a specific soluble guanylate cyclase homologue, gcy-35. The GCY-35 haem domain binds molecular oxygen, unlike the haem domains of classical nitric-oxide-regulated guanylate cyclases. GCY-35 and TAX-4 mediate oxygen sensation in four sensory neurons that control a naturally polymorphic social feeding behaviour in C. elegans. Social feeding and related behaviours occur only when oxygen exceeds C. elegans' preferred level, and require gcy-35 activity. Our results suggest that GCY-35 is regulated by molecular oxygen, and that social feeding can be a behavioural strategy for responding to hyperoxic environments.
Publication types
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Research Support, Non-U.S. Gov't
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Research Support, U.S. Gov't, Non-P.H.S.
MeSH terms
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Animals
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Bacteria / genetics
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Bacteria / metabolism
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Caenorhabditis elegans / drug effects
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Caenorhabditis elegans / enzymology*
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Caenorhabditis elegans / genetics
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Caenorhabditis elegans / physiology*
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Caenorhabditis elegans Proteins / chemistry
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Caenorhabditis elegans Proteins / genetics
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Caenorhabditis elegans Proteins / metabolism*
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Cell Aggregation / drug effects
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Cyclic GMP / metabolism
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Feeding Behavior / drug effects
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Feeding Behavior / physiology*
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Food
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Gases / metabolism
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Guanylate Cyclase / chemistry
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Guanylate Cyclase / genetics
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Guanylate Cyclase / metabolism*
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Heme / metabolism
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Hyperoxia / enzymology
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Hyperoxia / genetics
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Hyperoxia / metabolism
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Ion Channels / metabolism
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Mutation / genetics
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Neurons, Afferent / metabolism
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Nitric Oxide / metabolism
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Nitric Oxide / pharmacology
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Oxygen / metabolism*
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Oxygen / pharmacology
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Protein Binding
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Protein Structure, Tertiary
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Social Behavior*
Substances
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Caenorhabditis elegans Proteins
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Gases
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Ion Channels
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tax-4 protein, C elegans
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Nitric Oxide
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Heme
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GCY-35 protein, C elegans
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Guanylate Cyclase
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Cyclic GMP
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Oxygen