Abstract
Many nematodes show a stage-specific behavior called nictation in which a worm stands on its tail and waves its head in three dimensions. Here we show that nictation is a dispersal behavior regulated by a specific set of neurons, the IL2 cells, in C. elegans. We established assays for nictation and showed that cholinergic transmission was required for nictation. Cell type–specific rescue experiments and genetic ablation experiments revealed that the IL2 ciliated head neurons were essential for nictation. Intact cilia in IL2 neurons, but not in other ciliated head neurons, were essential, as the restoration of the corresponding wild-type gene activity in IL2 neurons alone in cilia-defective mutants was sufficient to restore nictation. Optogenetic activation of IL2 neurons induced nictation, suggesting that signals from IL2 neurons are sufficient for nictation. Finally, we demonstrated that nictation is required for transmission of C. elegans to a new niche using flies as artificial carriers, suggesting a role of nictation as a dispersal and survival strategy under harsh conditions.
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Change history
10 August 2012
In the version of this article initially published, the average durations for N2, cha-1(n2411) and cha-1(p503) shown in Figure 2b were incorrect because the n-values used to calculate them included cases in which no nictation was observed. The error has been corrected in the HTML and PDF versions of the article.
22 November 2013
Nat. Neurosci. 15, 107–112 (2012); published online 13 November 2011; corrected after print 10 August 2012 In the version of this article initially published, the average durations for N2, cha-1(n2411) and cha-1(p503) shown in Figure 2b (white bars) were incorrect because the n-values used to calculate them included cases in which no nictation was observed:
References
Reed, E.M. & Wallace, H.R. Leaping locomotion by an insect-parasitic nematode. Nature 206, 210–211 (1965).
Campbell, J.F. & Gaugler, R. Nictation behaviour and its ecological implications in the host search strategies of entomopathogenic nematodes (Heterorhabditidae and Steinernematidae). Behaviour 126, 155–169 (1993).
Evans, A.A.F. & Perry, R.N. Survival strategies in nematodes. in The Organization of Nematodes (ed. Croll, N.A.) 383–424 (Academic, London, 1976).
Croll, N.A. & Matthews, B.E. Biology of Nematodes (Blackie & Son, London, 1977).
Park, S. et al. Enhanced Caenorhabditis elegans locomotion in a structured microfluidic environment. PLoS ONE 3, e2550 (2008).
Lee, R.Y., Sawin, E.R., Chalfie, M., Horvitz, H.R. & Avery, L. EAT-4, a homolog of a mammalian sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in Caenorhabditis elegans. J. Neurosci. 19, 159–167 (1999).
Sze, J.Y., Victor, M., Loer, C., Shi, Y. & Ruvkun, G. Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403, 560–564 (2000).
Loer, C.M. & Kenyon, C.J. Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. J. Neurosci. 13, 5407–5417 (1993).
Kass, J., Jacob, T.C., Kim, P. & Kaplan, J.M. The EGL-3 proprotein convertase regulates mechanosensory responses of Caenorhabditis elegans. J. Neurosci. 21, 9265–9272 (2001).
Rand, J.B. & Russell, R.L. Choline acetyltransferase-deficient mutants of the nematode Caenorhabditis elegans. Genetics 106, 227–248 (1984).
McIntire, S.L., Jorgensen, E. & Horvitz, H.R. Genes required for GABA function in Caenorhabditis elegans. Nature 364, 334–337 (1993).
Rand, J.B. Genetic analysis of the cha-1-unc-17 gene complex in Caenorhabditis. Genetics 122, 73–80 (1989).
Nonet, M.L. et al. Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J. Neurosci. 17, 8061–8073 (1997).
Peden, E.M. & Barr, M.M. The KLP-6 kinesin is required for male mating behaviors and polycystin localization in Caenorhabditis elegans. Curr. Biol. 15, 394–404 (2005).
Ouellet, J., Li, S. & Roy, R. Notch signalling is required for both dauer maintenance and recovery in C. elegans. Development 135, 2583–2592 (2008).
Conradt, B. & Horvitz, H.R. The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 93, 519–529 (1998).
Chang, A.J., Chronis, N., Karow, D.S., Marletta, M.A. & Bargmann, C.I. A distributed chemosensory circuit for oxygen preference in C. elegans. PLoS Biol. 4, e274 (2006).
Ward, S., Thomson, N., White, J.G. & Brenner, S. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J. Comp. Neurol. 160, 313–337 (1975).
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).
Vowels, J.J. & Thomas, J.H. Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 130, 105–123 (1992).
Zhang, F., Wang, L.P., Boyden, E.S. & Deisseroth, K. Channelrhodopsin-2 and optical control of excitable cells. Nat. Methods 3, 785–792 (2006).
Barrière, A. & Felix, M.A. High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations. Curr. Biol. 15, 1176–1184 (2005).
Sudhaus, W. & Kuhne, R. Nematodes associated with Psychodidae: description of Rhabditis berolina sp. n. and redescription of R. dubia Bovien, 1937 (Nematoda: Rhabditidae), with biological and ecological notes, and a phylogenetic discussion. Nematologica 35, 305–320 (1989).
Albert, P.S. & Riddle, D.L. Developmental alterations in sensory neuroanatomy of the Caenorhabditis elegans dauer larva. J. Comp. Neurol. 219, 461–481 (1983).
Fayyazuddin, A., Zaheer, M.A., Hiesinger, P.R. & Bellen, H.J. The nicotinic acetylcholine receptor Dalpha7 is required for an escape behavior in Drosophila. PLoS Biol. 4, e63 (2006).
Yono, O. & Aonuma, H. Cholinergic neurotransmission from mechanosensory afferents to giant interneurons in the terminal abdominal ganglion of the cricket Gryllus bimaculatus. Zoolog. Sci. 25, 517–525 (2008).
Miller, M.W., Vu, E.T. & Krasne, F.B. Cholinergic transmission at the first synapse of the circuit mediating the crayfish lateral giant escape reaction. J. Neurophysiol. 68, 2174–2184 (1992).
Palikhova, T.A., Abramova, M.S. & Pivovarov, A.S. Cholinergic sensory inputs to command neurons in edible snail. Bull. Exp. Biol. Med. 142, 275–278 (2006).
Cassada, R.C. & Russell, R.L. The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev. Biol. 46, 326–342 (1975).
Chen, J., Lewis, E.E., Carey, J.R., Caswell, H. & Caswell-Chen, E.P. The ecology and biodemography of Caenorhabditis elegans. Exp. Gerontol. 41, 1059–1065 (2006).
Sivasundar, A. & Hey, J. Population genetics of Caenorhabditis elegans: the paradox of low polymorphism in a widespread species. Genetics 163, 147–157 (2003).
Barrière, A. & Felix, M.A. Natural variation and population genetics of Caenorhabditis elegans. WormBook 2005 1–19, (2005).
Darwin, C. On the Origin of Species (Murray, London, 1859).
Gittenberger, E., Groenenberg, D.S., Kokshoorn, B. & Preece, R.C. Biogeography: molecular trails from hitch-hiking snails. Nature 439, 409 (2006).
Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974).
MacQueen, A.J. et al. ACT-5 is an essential Caenorhabditis elegans actin required for intestinal microvilli formation. Mol. Biol. Cell 16, 3247–3259 (2005).
Golden, J.W. & Riddle, D.L. A Caenorhabditis elegans dauer-inducing pheromone and an antagonistic component of the food supply. J. Chem. Ecol. 10, 1265–1280 (1984).
Jeong, P.Y. et al. Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone. Nature 433, 541–545 (2005).
Butcher, R.A., Fujita, M., Schroeder, F.C. & Clardy, J. Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nat. Chem. Biol. 3, 420–422 (2007).
Xia, Y. & Whitesides, G.M. Soft lithography. Angew. Chem. Int. Edn. Engl. 37, 550–575 (1998).
Ramot, D., Johnson, B.E., Berry, T.L. Jr., Carnell, L. & Goodman, M.B. The Parallel Worm Tracker: a platform for measuring average speed and drug-induced paralysis in nematodes. PLoS ONE 3, e2208 (2008).
Mahoney, T.R., Luo, S. & Nonet, M.L. Analysis of synaptic transmission in Caenorhabditis elegans using an aldicarb-sensitivity assay. Nat. Protoc. 1, 1772–1777 (2006).
Hobert, O. PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32, 728–730 (2002).
Praitis, V., Casey, E., Collar, D. & Austin, J. Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157, 1217–1226 (2001).
Nagel, G. et al. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15, 2279–2284 (2005).
Acknowledgements
This work was initiated when J.L. was at his sabbatical leave in M. Han's laboratory (University of Colorado at Boulder). The authors thank Y. Kohara (National Institute of Genetics, Japan) for cDNA clones, A. Fire (Stanford University) for vectors, the J. Yim laboratory and the C.K. Chung laboratory (Seoul National University) for providing flies for our experiment, A. Gottschalk (Goethe University) for the ChR2 plasmid, P. Sengupta (Brandeis University) for the daf-10 cDNA plasmid and the Caenorhabditis Genetics Center for C. elegans strains. This work was supported by Brain Research Center of the 21st Century Frontier Research Program, the World Class University program and Research Center for Functional Cellulomics. M.C. was supported by Hi Seoul Science Fellowship from the Seoul Scholarship Foundation.
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H.L., M.C. and J.L. designed the study and wrote the paper; H.L., M.C. and D.L. performed experiments and analyzed the data; H.-s.K. performed the gauze test; H.H. and S.P. contributed to making the micro-dirt chip; H.-k.K. and Y.P. contributed to synthesizing pheromones. H.L. and M.C. contributed equally to the study. All authors discussed the results and commented on the manuscript.
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Supplementary information
Supplementary Text and Figures
Supplementary Figures 1–20 and Supplementary Tables 1–5 (PDF 1446 kb)
Supplementary Movie 1
A movie showing a dauer nictating on cotton medical gauze. Scale bar, 200 μm. (WMV 1328 kb)
Supplementary Movie 2
A movie showing a dauer nictating on the micro-dirt chip. Scale bar, 100 μm. (WMV 1145 kb)
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Lee, H., Choi, Mk., Lee, D. et al. Nictation, a dispersal behavior of the nematode Caenorhabditis elegans, is regulated by IL2 neurons. Nat Neurosci 15, 107–112 (2012). https://doi.org/10.1038/nn.2975
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DOI: https://doi.org/10.1038/nn.2975
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