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

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.

References

  1. 1

    Wu, R. S. Hypoxia: from molecular responses to ecosystem responses. Mar. Pollut. Bull. 45, 35–45 (2002)

    CAS  Article  Google Scholar 

  2. 2

    Wannamaker, C. M. & Rice, J. A. Effects of hypoxia on movements and behavior of selected estuarine organisms from the southeastern United States. J. Exp. Mar. Biol. Ecol. 249, 145–163 (2000)

    CAS  Article  Google Scholar 

  3. 3

    Sylvia, D. M., Fuhrmann, J. J., Hartel, P. G. & Zuberer, D. A. Principles and Applications of Soil Microbiology (Prentice Hall, Upper Saddle River, New Jersey, 1998)

    Google Scholar 

  4. 4

    Semenza, G. L. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 88, 1474–1480 (2000)

    CAS  Article  Google Scholar 

  5. 5

    Lopez-Barneo, J. Oxygen and glucose sensing by carotid body glomus cells. Curr. Opin. Neurobiol. 13, 493–499 (2003)

    CAS  Article  Google Scholar 

  6. 6

    Duffy, D. C., McDonald, J. C., Schueller, O. J. A. & Whitesides, G. M. Rapid prototyping of microfluidic systems in poly(dimethylsiloxane). Anal. Chem. 70, 4974–4984 (1998)

    CAS  Article  Google Scholar 

  7. 7

    Dusenbery, D. B. Appetitive response of the nematode Caenorhabditis elegans to oxygen. J. Comp. Physiol. 136, 333–336 (1980)

    Article  Google Scholar 

  8. 8

    Wingrove, J. A. & O'Farrell, P. H. Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98, 105–114 (1999)

    CAS  Article  Google Scholar 

  9. 9

    Hou, S. et al. Myoglobin-like aerotaxis transducers in Archaea and Bacteria. Nature 403, 540–544 (2000)

    ADS  CAS  Article  Google Scholar 

  10. 10

    Jain, R. & Chan, M. K. Mechanisms of ligand discrimination by heme proteins. J. Biol. Inorg. Chem. 8, 1–11 (2003)

    CAS  Article  Google Scholar 

  11. 11

    Yu, S., Avery, L., Baude, E. & Garbers, D. L. Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc. Natl Acad. Sci. USA 94, 3384–3387 (1997)

    ADS  CAS  Google Scholar 

  12. 12

    Morton, D. B., Hudson, M. L., Waters, E. & O'Shea, M. Soluble guanylyl cyclases in Caenorhabditis elegans: NO is not the answer. Curr. Biol. 9, R546–R547 (1999)

    CAS  Article  Google Scholar 

  13. 13

    Morton, D. B. Invertebrates yield a plethora of atypical guanylyl cyclases. Mol. Neurobiol. 29, 97–116 (2004)

    CAS  Article  Google Scholar 

  14. 14

    Finn, J. T., Grunwald, M. E. & Yau, K. W. Cyclic nucleotide-gated ion channels: an extended family with diverse functions. Annu. Rev. Physiol. 58, 395–426 (1996)

    CAS  Article  Google Scholar 

  15. 15

    Coburn, C. M. & Bargmann, C. I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17, 695–706 (1996)

    CAS  Article  Google Scholar 

  16. 16

    Komatsu, H., Mori, I., Rhee, J. S., Aiakie, N. & Ohshima, Y. Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17, 707–718 (1996)

    CAS  Article  Google Scholar 

  17. 17

    Zhao, Y. & Marletta, M. A. Localization of the heme binding region in soluble guanylate cyclase. Biochemistry 36, 15959–15964 (1997)

    CAS  Article  Google Scholar 

  18. 18

    Coates, J. C. & de Bono, M. Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans. Nature 419, 925–929 (2002)

    ADS  CAS  Article  Google Scholar 

  19. 19

    de Bono, M. & Bargmann, C. I. Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94, 679–689 (1998)

    CAS  Article  Google Scholar 

  20. 20

    Rogers, C. et al. Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nature Neurosci. 6, 1178–1185 (2003)

    CAS  Article  Google Scholar 

  21. 21

    de Bono, M., Tobin, D. M., Davis, M. W., Avery, L. & Bargmann, C. I. Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli. Nature 419, 899–903 (2002)

    ADS  CAS  Article  Google Scholar 

  22. 22

    Cheung, B. H. H., Arellano-Carbajal, F., Rybicki, I. & de Bono, M. Soluble guanylate cyclases act in neurons exposed to the body fluid to promote C. elegans aggregation behaviour. Curr. Biol. (in the press)

  23. 23

    Malinski, T. & Taha, Z. Nitric oxide release from a single cell measured in situ by a porphyrinic-based microsensor. Nature 358, 676–678 (1992)

    ADS  CAS  Article  Google Scholar 

  24. 24

    Malinski, T., Taha, Z. & Grunfeld, S. Diffusion of nitric oxide in the aorta wall monitored in situ by porphyrinic microsensors. Biochem. Biophys. Res. Commun. 193, 1076–1082 (1993)

    CAS  Article  Google Scholar 

  25. 25

    Karow, D. S. et al. Spectroscopic characterization of the sGC-like heme domains from Vibrio cholerae and Thermoanaerobacter tengcongensis. Biochemistry (in the press)

  26. 26

    White, J., Southgate, E., Thomson, J. N. & Brenner, S. The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. B 314, 1–340 (1986)

    ADS  CAS  Article  Google Scholar 

  27. 27

    Van Voorhies, W. A. & Ward, S. Broad oxygen tolerance in the nematode Caenorhabditis elegans. J. Exp. Biol. 203, 2467–2478 (2000)

    CAS  PubMed  Google Scholar 

  28. 28

    Anderson, G. L. & Dusenbery, D. B. Critical oxygen tension of Caenorhabditis elegans. J. Nematol. 9, 253–254 (1977)

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29

    Imlay, J. A. Pathways of oxidative damage. Annu. Rev. Microbiol. 57, 395–418 (2003)

    CAS  Article  Google Scholar 

  30. 30

    Barak, R., Nur, I., Okon, Y. & Henis, Y. Aerotactic response of Azospirillum brasilense. J. Bacteriol. 152, 643–649 (1982)

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31

    Hieb, W. F., Stokstad, E. L. & Rothstein, M. Heme requirement for reproduction of a free-living nematode. Science 168, 143–144 (1970)

    ADS  CAS  Article  Google Scholar 

  32. 32

    Stone, J. R. & Marletta, M. A. Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and rerric States. Biochemistry 33, 5636–5640 (1994)

    CAS  Article  Google Scholar 

  33. 33

    Di Iorio, E. E. in Hemoglobins (eds Antonini, E., Rossi-Bernardi, L. & Chiancone, E.) 57–71 (Academic, New York, 1981)

    Google Scholar 

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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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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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