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Molecular basis of infrared detection by snakes

Naturevolume 464, pages1006–1011 (2010)Cite this article

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Abstract

Snakes possess a unique sensory system for detecting infrared radiation, enabling them to generate a ‘thermal image’ of predators or prey. Infrared signals are initially received by the pit organ, a highly specialized facial structure that is innervated by nerve fibres of the somatosensory system. How this organ detects and transduces infrared signals into nerve impulses is not known. Here we use an unbiased transcriptional profiling approach to identify TRPA1 channels as infrared receptors on sensory nerve fibres that innervate the pit organ. TRPA1 orthologues from pit-bearing snakes (vipers, pythons and boas) are the most heat-sensitive vertebrate ion channels thus far identified, consistent with their role as primary transducers of infrared stimuli. Thus, snakes detect infrared signals through a mechanism involving radiant heating of the pit organ, rather than photochemical transduction. These findings illustrate the broad evolutionary tuning of transient receptor potential (TRP) channels as thermosensors in the vertebrate nervous system.

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Figure 1:Anatomy of the pit organ and comparison of gene expression in snake sensory ganglia.
Figure 2:Expression of TRPA1 and TRPV1 in rattlesnake sensory ganglia.
Figure 3:Functional analysis of snake TRPA1 channels.
Figure 4:Analysis of TRPA1 from python and boa.
Figure 5:Functional analysis of snake sensory neurons.

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Accession codes

Primary accessions

Gene Expression Omnibus

Data deposits

Deep sequencing data are archived under GEO accession numberGSE19911. GenBank accession numbers are GU562965 (Python regius TRPA1), GU562966 (Elaphe obsoleta lindheimeri TRPA1), GU562967 (Crotalus atrox TRPA1), GU562968 (Crotalus atrox TRPV1), and GU562969 (Corallus hortulanus TRPA1).

Change history

  • 15 April 2010

    A correction was made to the spelling of an author name (N.T.I.) on 15 April.

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Acknowledgements

We thank A. Priel for advice and assistance with calcium imaging and electrophysiology, C. Chu for help with sequencing, J. Poblete for technical assistance, and the staff of the Natural Toxins Research Center serpentarium for animal husbandry. We thank P. Garrity for providing the dTrpA1 cDNA. This work was supported by a Ruth L. Kirschstein National Research Service Award (GM080853) (N.T.I.), a NIH Institutional Research Service Award in Molecular and Cellular Basis of Cardiovascular Disease (A.T.C.), the Howard Hughes Medical Institute (J.S.W.), and grants from the National Institutes of Health, including NCRR Viper grant P40 RR018300-06 (E.E.S. and J.C.P.), P01 AG010770 (J.S.W.) and NS047723 and NS055299 (D.J.).

Author Contributions E.O.G., J.F.C.-M. and N.T.I. designed and performed experiments and analysed data. N.T.I. and J.S.W. developed analytical tools and analysed data. Y.M.K., G.H. and A.T.C. performed experiments and/or provided reagents and analysed data. E.E.S. and J.C.P. supervised snake husbandry and handling. E.O.G., Y.M.K., J.F.C.-M. and D.J. wrote the manuscript with discussion and contributions from all authors. J.S.W. and D.J. provided advice and guidance throughout. D.J. initiated and supervised the project.

Author information

Author notes

  1. Gunther Hollopeter

    Present address: Present address: Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City, Utah 84112-0840, USA.,

  2. Elena O. Gracheva and Nicholas T. Ingolia: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Physiology,,

    Elena O. Gracheva, Yvonne M. Kelly, Julio F. Cordero-Morales, Gunther Hollopeter, Alexander T. Chesler & David Julius

  2. Department of Cellular and Molecular Pharmacology,,

    Nicholas T. Ingolia, Jonathan S. Weissman & David Julius

  3. Howard Hughes Medical Institute,,

    Nicholas T. Ingolia & Jonathan S. Weissman

  4. California Institute for Quantitative Biosciences, University of California, San Francisco, California 94158-2517, USA ,

    Nicholas T. Ingolia & Jonathan S. Weissman

  5. Natural Toxins Research Center, Texas A&M University- Kingsville, Texas 78363, USA

    Elda E. Sánchez & John C. Perez

Authors
  1. Elena O. Gracheva
  2. Nicholas T. Ingolia
  3. Yvonne M. Kelly
  4. Julio F. Cordero-Morales
  5. Gunther Hollopeter
  6. Alexander T. Chesler
  7. Elda E. Sánchez
  8. John C. Perez
  9. Jonathan S. Weissman
  10. David Julius

Corresponding author

Correspondence toDavid Julius.

Supplementary information

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Gracheva, E., Ingolia, N., Kelly, Y.et al. Molecular basis of infrared detection by snakes.Nature464, 1006–1011 (2010). https://doi.org/10.1038/nature08943

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Editorial Summary

Thermal imaging by snakes

Only four vertebrate species are known to possess the 'sixth sense' of infrared detection, which is used for both predatory and thermoregulatory purposes. These creatures include three distantly related species of snake (pit vipers, pythons and boas) and the vampire bats. The pit organ that mediates this sense has been extensively studied from anatomical and behavioural perspectives, but little is known about the signal transduction mechanism underlying infrared detection, or the molecules involved. Now Grachevaet al. show that pit-bearing snakes rely on exquisite heat detection by the ion channel TRPA1. This extends the sensory repertoire of TRPA1 family of proteins, which detect chemical irritants in mammals and thermal variations in insects.

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