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Light-sensitive neurons and channels mediate phototaxis in C. elegans

Abstract

Phototaxis behavior is commonly observed in animals with light-sensing organs. C. elegans, however, is generally believed to lack phototaxis, as this animal lives in darkness (soil) and does not possess eyes. Here, we found that light stimuli elicited negative phototaxis in C. elegans and that this behavior is important for survival. We identified a group of ciliary sensory neurons as candidate photoreceptor cells for mediating phototaxis. Furthermore, we found that light excited photoreceptor cells by evoking a depolarizing conductance carried by cyclic guanosine monophosphate (cGMP)-sensitive cyclic nucleotide–gated (CNG) channels, revealing a conservation in phototransduction between worms and vertebrates. These results identify a new sensory modality in C. elegans and suggest that animals living in dark environments without light-sensing organs may not be presumed to be light insensitive. We propose that urbilaterians, the last common ancestor of bilaterians, might have already evolved a visual system that employs CNG channels and the second messenger cGMP for phototransduction.

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Figure 1: Light evokes avoidance responses in C. elegans in a dose-dependent manner.
Figure 2: Behavioral quantification of phototactic responses.
Figure 3: Prolonged light exposure induces paralysis/lethality in worms.
Figure 4: Phototaxis in C. elegans requires ciliary sensory neurons and CNG channels.
Figure 5: Light stimulates the photoreceptor neuron ASJ by evoking an inward current carried by CNG channels.
Figure 6: The light-sensitive CNG channels in the photoreceptor neuron ASJ are sensitive to cGMP.

References

  1. Kandel, E.R. The neurobiology of behavior. in Principles of Neural Science (eds. Kandel, E.R., Schwartz, J.H. & Jessell, T.M.) 5–66 (McGraw-Hill Medical, 2000).

    Google Scholar 

  2. Bargmann, C.I. Comparative chemosensation from receptors to ecology. Nature 444, 295–301 (2006).

    CAS  Article  PubMed  Google Scholar 

  3. Fu, Y. & Yau, K.W. Phototransduction in mouse rods and cones. Pflugers Arch. 454, 805–819 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Wang, T. & Montell, C. Phototransduction and retinal degeneration in Drosophila. Pflugers Arch. 454, 821–847 (2007).

    CAS  Article  PubMed  Google Scholar 

  5. Berson, D.M. Phototransduction in ganglion-cell photoreceptors. Pflugers Arch. 454, 849–855 (2007).

    CAS  Article  PubMed  Google Scholar 

  6. Kelber, A., Vorobyev, M. & Osorio, D. Animal color vision–behavioral tests and physiological concepts. Biol. Rev. Camb. Philos. Soc. 78, 81–118 (2003).

    Article  PubMed  Google Scholar 

  7. Bargmann, C.I. Chemosensation. in C. elegans. WormBook, 1–29〈http://www.wormbook.org/〉 (2006).

    Google Scholar 

  8. Bounoutas, A. & Chalfie, M. Touch sensitivity in Caenorhabditis elegans. Pflugers Arch. 454, 691–702 (2007).

    CAS  Article  PubMed  Google Scholar 

  9. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Burr, A.H. The photomovement of Caenorhabditis elegans, a nematode which lacks ocelli. Proof that the response is to light not radiant heating. Photochem. Photobiol. 41, 577–582 (1985).

    CAS  Article  PubMed  Google Scholar 

  11. Harris, W.A., Stark, W.S. & Walker, J.A. Genetic dissection of the photoreceptor system in the compound eye of Drosophila melanogaster. J. Physiol. (Lond.) 256, 415–439 (1976).

    CAS  Article  Google Scholar 

  12. White, J.G., 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).

    CAS  Article  Google Scholar 

  13. Gabel, C.V. et al. Neural circuits mediate electrosensory behavior in Caenorhabditis elegans. J. Neurosci. 27, 7586–7596 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Kaupp, U.B. & Seifert, R. Cyclic nucleotide–gated ion channels. Physiol. Rev. 82, 769–824 (2002).

    CAS  Article  PubMed  Google Scholar 

  15. Cho, S.W., Cho, J.H., Song, H.O. & Park, C.S. Identification and characterization of a putative cyclic nucleotide–gated channel, CNG-1, in C. elegans. Mol. Cells 19, 149–154 (2005).

    CAS  PubMed  Google Scholar 

  16. Komatsu, H. et al. Functional reconstitution of a heteromeric cyclic nucleotide–gated channel of Caenorhabditis elegans in cultured cells. Brain Res. 821, 160–168 (1999).

    CAS  Article  PubMed  Google Scholar 

  17. 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  PubMed  Google Scholar 

  18. Finn, J.T., Solessio, E.C. & Yau, K.W. A cGMP-gated cation channel in depolarizing photoreceptors of the lizard parietal eye. Nature 385, 815–819 (1997).

    CAS  Article  PubMed  Google Scholar 

  19. Stern, J.H., Kaupp, U.B. & MacLeish, P.R. Control of the light-regulated current in rod photoreceptors by cyclic GMP, calcium, and l–cis-diltiazem. Proc. Natl. Acad. Sci. USA 83, 1163–1167 (1986).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 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).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Mulsch, A., Luckhoff, A., Pohl, U., Busse, R. & Bassenge, E. LY 83583 (6-anilino-5,8-quinolinedione) blocks nitrovasodilator-induced cyclic GMP increases and inhibition of platelet activation. Naunyn Schmiedebergs Arch. Pharmacol. 340, 119–125 (1989).

    CAS  PubMed  Google Scholar 

  22. Danziger, R.S. et al. Characterization of soluble guanylyl cyclase in transformed human nonpigmented epithelial cells. Biochem. Biophys. Res. Commun. 195, 958–962 (1993).

    CAS  Article  PubMed  Google Scholar 

  23. Bargmann, C.I., Hartwieg, E. & Horvitz, H.R. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74, 515–527 (1993).

    CAS  Article  PubMed  Google Scholar 

  24. Ward, S. Chemotaxis by the nematode Caenorhabditis elegans: identification of attractants and analysis of the response by use of mutants. Proc. Natl. Acad. Sci. USA 70, 817–821 (1973).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Gray, J.M. et al. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430, 317–322 (2004).

    CAS  Article  PubMed  Google Scholar 

  26. Chalfie, M. et al. The neural circuit for touch sensitivity in Caenorhabditis elegans. J. Neurosci. 5, 956–964 (1985).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Kaplan, J.M. & Horvitz, H.R. A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 90, 2227–2231 (1993).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. Cheung, B.H., Cohen, M., Rogers, C., Albayram, O. & de Bono, M. Experience-dependent modulation of C. elegans behavior by ambient oxygen. Curr. Biol. 15, 905–917 (2005).

    CAS  Article  PubMed  Google Scholar 

  29. Salvini-Plawen, L. & Mayr, E. On the evolution of photoreceptors and eyes. in Evolutionary Biology (eds. Hecht, M.K., Steere, W.C. & Wallace, B.) 207–273 (Plenum Press, New York, 1961).

    Google Scholar 

  30. Gehring, W.J. & Ikeo, K. Pax 6: mastering eye morphogenesis and eye evolution. Trends Genet. 15, 371–377 (1999).

    CAS  Article  PubMed  Google Scholar 

  31. Gehring, W.J. New perspectives on eye development and the evolution of eyes and photoreceptors. J. Hered. 96, 171–184 (2005).

    CAS  Article  PubMed  Google Scholar 

  32. Arendt, D., Tessmar, K., de Campos-Baptista, M.I., Dorresteijn, A. & Wittbrodt, J. Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria. Development 129, 1143–1154 (2002).

    CAS  PubMed  Google Scholar 

  33. Chitwood, B.G. & Murphy, D.G. Observations on two marine monhysterids: their classification, cultivation, and behavior. Trans. Am. Microsc. Soc. 83, 311–329 (1964).

    Article  Google Scholar 

  34. Croll, N.A. The phototactic response and spectral sensitivity of Chromadorina viridis (Nematoda, Chromadorida) with a note on the nature of the paired pigment spots. Nematologica 12, 610–614 (1966).

    CAS  Article  Google Scholar 

  35. Montell, C. Visual transduction in Drosophila. Annu. Rev. Cell Dev. Biol. 15, 231–268 (1999).

    CAS  Article  PubMed  Google Scholar 

  36. Adoutte, A., Balavoine, G., Lartillot, N. & de Rosa, R. Animal evolution. The end of the intermediate taxa? Trends Genet. 15, 104–108 (1999).

    CAS  Article  PubMed  Google Scholar 

  37. Gray, J.M., Hill, J.J. & Bargmann, C.I. A circuit for navigation in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 102, 3184–3191 (2005).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Li, W., Feng, Z., Sternberg, P.W. & Xu, X.Z.S.A. C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440, 684–687 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Feng, Z. et al. A C. elegans model of nicotine-dependent behavior: regulation by TRP family channels. Cell 127, 621–633 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Bargmann, C.I. & Avery, L. Laser killing of cells in Caenorhabditis elegans. Methods Cell Biol. 48, 225–250 (1995).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Troemel, E.R., Chou, J.H., Dwyer, N.D., Colbert, H.A. & Bargmann, C.I. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83, 207–218 (1995).

    CAS  Article  PubMed  Google Scholar 

  42. Miranda-Vizuete, A. et al. Lifespan decrease in a Caenorhabditis elegans mutant lacking TRX-1, a thioredoxin expressed in ASJ sensory neurons. FEBS Lett. 580, 484–490 (2006).

    CAS  Article  PubMed  Google Scholar 

  43. Richmond, J.E. & Jorgensen, E.M. One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction. Nat. Neurosci. 2, 791–797 (1999).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Brockie, P.J., Mellem, J.E., Hills, T., Madsen, D.M. & Maricq, A.V. The C. elegans glutamate receptor subunit NMR-1 is required for slow NMDA-activated currents that regulate reversal frequency during locomotion. Neuron 31, 617–630 (2001).

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

We thank P. Hu and A. Kumar for comments; C. Bargmann for providing tax-2 rescuing strains; B. Decaluwe, M. Xia and S. Gu for technical assistance; L. Kang for movie editing; Q. Liu and Z.W. Wang for assistance in setting up recording; and members of the Xu lab for advice. Some strains were obtained from the Caenorhabditis Genetics Center. A.W. was supported by a US National Institutes of Health predoctoral training grant. This work was supported by the US National Institute of General Medical Sciences (NIGMS) and the Pew scholars program (X.Z.S.X.).

Author information

Authors and Affiliations

Authors

Contributions

A.W. conducted the experiments and analyzed the data in Figures 1, 2, 3, 4. J.L. conducted the experiments and analyzed the data in Figures 5 and 6. Z.F. developed tools to acquire and analyze behavioral data. X.Z.S.X. supervised the project and wrote the manuscript.

Corresponding author

Correspondence to X Z Shawn Xu.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–6 (PDF 135 kb)

Supplementary Video 1

Head avoidance response. The movie is in AVI format. The animal was in forward motion at the beginning. At 5.80 s, a flash of light (2 s duration, A) was turned on. At 7.05 s, the animal paused and initiated backward movement that lasted for seven head swings, followed by an omega turn. The stage was moved manually during recording to keep the worm in the view field. (AVI 7499 kb)

Supplementary Video 2

Tail avoidance response. The movie is in AVI format. At 1.72 s, a flash of light (2 s duration, UV-A) was turned on. At 2.85 s, the worm responded by stopping backward movement and beginning to move forward. The stage was moved manually during recording to keep the worm in the view field. Light shed on the tail or body of a worm in forward motion would further stimulate its forward movement. (AVI 3851 kb)

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Ward, A., Liu, J., Feng, Z. et al. Light-sensitive neurons and channels mediate phototaxis in C. elegans. Nat Neurosci 11, 916–922 (2008). https://doi.org/10.1038/nn.2155

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