1. Howard Hughes Medical Institute and Departments of Anatomy and Biochemistry and Biophysics, The University of California, San Francisco, California 94143-0452, USA
2. Graduate Program in Cellular and Molecular Biology, University of Michigan, Ann Arbor, Michigan 48109, USA
3. Department of Chemistry, University of Michigan, Ann Arbor, Michigan 48109, USA
4. UMDNJ School of Osteopathic Medicine, Stratford, New Jersey 08084, USA
5. Departments of Chemistry and Molecular and Cell Biology, the University of California, Berkeley, CA 94720-1460, USA
6. The Division of Physical Biosciences, Lawrence Berkeley National Lab, Berkeley, California 94720, USA
7. These authors contributed equally to this work

Correspondence to: Michael A. Marletta^5,6Cornelia I. Bargmann¹ Email: cori@itsa.ucsf.edu
Email: marletta@berkeley.edu

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.

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