Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue

Nature. 2004 Jul 15;430(6997):317-22. doi: 10.1038/nature02714. Epub 2004 Jun 27.

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

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Bacteria / genetics
  • Bacteria / metabolism
  • Caenorhabditis elegans / drug effects
  • Caenorhabditis elegans / enzymology*
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / chemistry
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Aggregation / drug effects
  • Cyclic GMP / metabolism
  • Feeding Behavior / drug effects
  • Feeding Behavior / physiology*
  • Food
  • Gases / metabolism
  • Guanylate Cyclase / chemistry
  • Guanylate Cyclase / genetics
  • Guanylate Cyclase / metabolism*
  • Heme / metabolism
  • Hyperoxia / enzymology
  • Hyperoxia / genetics
  • Hyperoxia / metabolism
  • Ion Channels / metabolism
  • Mutation / genetics
  • Neurons, Afferent / metabolism
  • Nitric Oxide / metabolism
  • Nitric Oxide / pharmacology
  • Oxygen / metabolism*
  • Oxygen / pharmacology
  • Protein Binding
  • Protein Structure, Tertiary
  • Social Behavior*

Substances

  • Caenorhabditis elegans Proteins
  • Gases
  • Ion Channels
  • tax-4 protein, C elegans
  • Nitric Oxide
  • Heme
  • GCY-35 protein, C elegans
  • Guanylate Cyclase
  • Cyclic GMP
  • Oxygen