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

Jesse M. Gray, David S. Karow, Hang Lu, Andy J. Chang, Jennifer S. Chang, Ronald E. Ellis, Michael A. Marletta () and Cornelia I. Bargmann ()
Additional contact information
Jesse M. Gray: The University of California
David S. Karow: University of Michigan
Hang Lu: The University of California
Andy J. Chang: The University of California
Jennifer S. Chang: University of Michigan
Ronald E. Ellis: UMDNJ School of Osteopathic Medicine
Michael A. Marletta: the University of California
Cornelia I. Bargmann: The University of California

Nature, 2004, vol. 430, issue 6997, 317-322

Abstract: 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.

Date: 2004
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DOI: 10.1038/nature02714

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