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

Nature volume 430, pages 317–322 (2004)Cite this article

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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Figure 1: gcy-35 mutants are defective in hyperoxia avoidance.
Figure 2: gcy-35::gfp is expressed in URX, AQR, PQR and other sensory neurons.
Figure 3: Characterization of GCY-35(1–252) binding to gases.
Figure 4: Oxygen stimulates GCY-35-dependent aggregation and bordering.
Figure 5: Regulation of oxygen responses by food.

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Acknowledgements

We thank J. Feldman for discussions and contributions to the aerotaxis assay, M. Hudson and D. Morton for advice and discussions, C. Ross, S. Nicholls and M. Miazgowicz for technical assistance, M. Zimmer for the gcy-32 promoter, S. McCarroll for the pSM1 vector, the C. elegans Knockout Consortium and Caenorhabditis Genetics Center (CGC) for the gcy-35(ok769) mutant strain, and B. Cheung and M. de Bono for sharing their results before publication. J.M.G. was supported by a Howard Hughes Medical Institute Predoctoral Fellowship. A.J.C. was supported by an NSF Predoctoral Fellowship. C.I.B. is an Investigator of the Howard Hughes Medical Institute. This work was supported by funding from the Howard Hughes Medical Institute (to C.I.B.) and by the LDRD fund from the Lawrence Berkeley National Lab (to M.A.M.).

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Author notes

  1. Jesse M. Gray and David S. Karow: These authors contributed equally to this work

Authors and Affiliations

  1. Howard Hughes Medical Institute and Departments of Anatomy and Biochemistry and Biophysics, The University of California, San Francisco, California, 94143-0452, USA

    Jesse M. Gray, Hang Lu, Andy J. Chang & Cornelia I. Bargmann

  2. Graduate Program in Cellular and Molecular Biology, University of Michigan, Ann Arbor, Michigan, 48109, USA

    David S. Karow

  3. Department of Chemistry, University of Michigan, Ann Arbor, Michigan, 48109, USA

    Jennifer S. Chang

  4. UMDNJ School of Osteopathic Medicine, Stratford, New Jersey, 08084, USA

    Ronald E. Ellis

  5. Departments of Chemistry and Molecular and Cell Biology, the University of California, Berkeley, CA 94720-1460, USA

    Michael A. Marletta

  6. The Division of Physical Biosciences, Lawrence Berkeley National Lab, Berkeley, California, 94720, USA

    Michael A. Marletta

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Correspondence to Michael A. Marletta or Cornelia I. Bargmann.

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Supplementary information

Supplementary Figure 1

Comparison of C. elegans GCY sequences and mammalian soluble guanylate cyclase sequences. (PDF 254 kb)

Supplementary Figure 2

Statistical analysis of aerotaxis data in Figure 1 and other aerotaxis results. (PDF 225 kb)

Supplementary Figure 3

Aerotaxis results for gcy-35 rescuing strains and for tax-2 and tax-4 mutants, and oxygen-regulated behaviors in tax-4 mutants and double mutants. (PDF 365 kb)

Supplementary Figure Legends

Legends for Supplementary Figures 1–3 and additional references. (DOC 34 kb)

Supplementary Methods

This includes a detailed description of the Methods and additional references. (DOC 39 kb)

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Gray, J., Karow, D., Lu, H. et al. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430, 317–322 (2004). https://doi.org/10.1038/nature02714

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