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

Author

Listed:
  • 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
    Lawrence Berkeley National Lab)

  • Cornelia I. Bargmann

    (The University of California)

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.

Suggested Citation

  • Jesse M. Gray & David S. Karow & Hang Lu & Andy J. Chang & Jennifer S. Chang & Ronald E. Ellis & Michael A. Marletta & Cornelia I. Bargmann, 2004. "Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue," Nature, Nature, vol. 430(6997), pages 317-322, July.
    • Handle: RePEc:nat:nature:v:430:y:2004:i:6997:d:10.1038_nature02714
    DOI: 10.1038/nature02714
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    Cited by:

    1. Mara H. Cowen & Dustin Haskell & Kristi Zoga & Kirthi C. Reddy & Sreekanth H. Chalasani & Michael P. Hart, 2024. "Conserved autism-associated genes tune social feeding behavior in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Saurabh Thapliyal & Isabel Beets & Dominique A. Glauser, 2023. "Multisite regulation integrates multimodal context in sensory circuits to control persistent behavioral states in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

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