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

Nature Neuroscience volume 11, pages 916–922 (2008)Cite this article

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.

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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

Author notes

  1. Zhaoyang Feng

    Present address: Present address: Department of Pharmacology, Case Western Reserve University, 10900 Euclid Ave, Cleveland, Ohio 44106, USA.,

  2. Alex Ward and Jie Liu: These authors contributed equally to this work.

Authors and Affiliations

  1. Life Sciences Institute, University of Michigan, 210 Washtenaw Avenue, Ann Arbor, 48109, Michigan, USA

    Alex Ward, Jie Liu, Zhaoyang Feng & X Z Shawn Xu

  2. Neuroscience Graduate Program, University of Michigan, 210 Washtenaw Avenue, Ann Arbor, 48109, Michigan, USA

    Alex Ward & X Z Shawn Xu

  3. Department of Molecular and Integrative Physiology, University of Michigan, 210 Washtenaw Avenue, Ann Arbor, 48109, Michigan, USA

    X Z Shawn Xu

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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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