Abstract
Humans and other animals can sense temperature changes as small as 0.1 °C. How animals achieve such exquisite sensitivity is poorly understood. By recording from the C. elegans thermosensory neurons AFD in vivo, we found that cooling closes and warming opens ion channels. We found that AFD thermosensitivity, which exceeds that of most biological processes by many orders of magnitude, is achieved by nonlinear signal amplification. Mutations in genes encoding subunits of a cyclic guanosine monophosphate (cGMP)-gated ion channel (tax-4 and tax-2) and transmembrane guanylate cyclases (gcy-8, gcy-18 and gcy-23) eliminated both cooling- and warming-activated thermoreceptor currents, indicating that a cGMP-mediated pathway links variations in temperature to changes in ionic currents. The resemblance of C. elegans thermosensation to vertebrate photosensation and the sequence similarity between TAX-4 and TAX-2 and subunits of the rod phototransduction channel raise the possibility that nematode thermosensation and vertebrate vision are linked by conserved evolution.
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Acknowledgements
We thank C.F. Barrett, T.R. Clandinin, J. Huegenard, A.Y. Katsov, S. Lockery, R. Milo and the Goodman laboratory for comments; G. Wang and Z. Liao for help with genotyping; and P. Sengupta, C. Bargmann, I. Mori and the Caenorhabditis Genetics Center, which is funded by the US National Institutes of Health National Center for Research Resources, for strains. This work was supported by the Baxter, Sloan, McKnight and Klingenstein Foundations (M.B.G.), the National Science Foundation (M.B.G.), the US National Institutes of Health (M.B.G.), a fellowship from the Human Frontiers Science Program (B.L.M.), and a Stanford Graduate Fellowship and Dan David Prize Scholarship (D.R.).
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D.R. conducted electrophysiology experiments, analyzed data and wrote the manuscript. B.L.M. prepared mutant strains, conducted behavioral experiments and contributed to writing the manuscript. M.B.G. conducted electrophysiology experiments, supervised the project and wrote the manuscript.
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Ramot, D., MacInnis, B. & Goodman, M. Bidirectional temperature-sensing by a single thermosensory neuron in C. elegans. Nat Neurosci 11, 908–915 (2008). https://doi.org/10.1038/nn.2157
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DOI: https://doi.org/10.1038/nn.2157
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