Abstract
Blood-feeding insects, including the malaria mosquito Anopheles gambiae, use highly specialized and sensitive olfactory systems to locate their hosts. This is accomplished by detecting and following plumes of volatile host emissions, which include carbon dioxide (CO2)1. CO2 is sensed by a population of olfactory sensory neurons in the maxillary palps of mosquitoes2,3 and in the antennae of the more genetically tractable fruitfly, Drosophila melanogaster4. The molecular identity of the chemosensory CO2 receptor, however, remains unknown. Here we report that CO2-responsive neurons in Drosophila co-express a pair of chemosensory receptors, Gr21a and Gr63a, at both larval and adult life stages. We identify mosquito homologues of Gr21a and Gr63a, GPRGR22 and GPRGR24, and show that these are co-expressed in A. gambiae maxillary palps. We show that Gr21a and Gr63a together are sufficient for olfactory CO2-chemosensation in Drosophila. Ectopic expression of Gr21a and Gr63a together confers CO2 sensitivity on CO2-insensitive olfactory neurons, but neither gustatory receptor alone has this function. Mutant flies lacking Gr63a lose both electrophysiological and behavioural responses to CO2. Knowledge of the molecular identity of the insect olfactory CO2 receptors may spur the development of novel mosquito control strategies designed to take advantage of this unique and critical olfactory pathway. This in turn could bolster the worldwide fight against malaria and other insect-borne diseases.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Gillies, M. T. The role of carbon dioxide in host-finding in mosquitoes (Diptera:Culicidae): a review. Bull. Entomol. Res. 70, 525–532 (1980)
Kellogg, F. E. Water vapour and carbon dioxide receptors in Aedes aegypti. J. Insect Physiol. 16, 99–108 (1970)
Grant, A. J., Wigton, B. E., Aghajanian, J. G. & O’Connell, R. J. Electrophysiological responses of receptor neurons in mosquito maxillary palp sensilla to carbon dioxide. J. Comp. Physiol. A 177, 389–396 (1995)
de Bruyne, M., Foster, K. & Carlson, J. R. Odor coding in the Drosophila antenna. Neuron 30, 537–552 (2001)
Nicolas, G. & Sillans, D. Immediate and latent effects of carbon dioxide on insects. Annu. Rev. Entomol. 34, 97–116 (1989)
Thom, C., Guerenstein, P. G., Mechaber, W. L. & Hildebrand, J. G. Floral CO2 reveals flower profitability to moths. J. Chem. Ecol. 30, 1285–1288 (2004)
Southwick, E. E. & Moritz, R. F. A. Social control of air ventilation in colonies of honey bees, Apis mellifera. J. Insect Physiol. 33, 623–626 (1987)
Takken, W. & Knols, B. G. Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu. Rev. Entomol. 44, 131–157 (1999)
Suh, G. S. et al. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431, 854–859 (2004)
Faucher, C., Forstreuter, M., Hilker, M. & de Bruyne, M. Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context. J. Exp. Biol. 209, 2739–2748 (2006)
Stange, G. & Stowe, S. Carbon-dioxide sensing structures in terrestrial arthropods. Microsc. Res. Tech 47, 416–427 (1999)
Scott, K. et al. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661–673 (2001)
Robertson, H. M., Warr, C. G. & Carlson, J. R. Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 100, (Suppl. 2)14537–14542 (2003)
Wang, Z., Singhvi, A., Kong, P. & Scott, K. Taste representations in the Drosophila brain. Cell 117, 981–991 (2004)
Fishilevich, E. & Vosshall, L. B. Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15, 1548–1553 (2005)
Hill, C. A. et al. G protein-coupled receptors in Anopheles gambiae. Science 298, 176–178 (2002)
Dobritsa, A. A. van der Goes van Naters, W. Warr, C. G., Steinbrecht, R. A. & Carlson, J. R. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37, 827–841 (2003)
Benton, R., Sachse, S., Michnick, S. W. & Vosshall, L. B. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol. 4, e20 (2006)
Hallem, E. A. & Carlson, J. R. Coding of odors by a receptor repertoire. Cell 125, 143–160 (2006)
Shanbhag, S. R., Mueller, B. & Steinbrecht, R. A. Atlas of olfactory organs of Drosophila melanogaster. 1. Types, external organization, innervation and distribution of olfactory sensilla. Int. J. Insect Morphol. Embryol. 28, 377–397 (1999)
Gong, W. J. & Golic, K. G. Ends-out, or replacement, gene targeting in Drosophila. Proc. Natl Acad. Sci. USA 100, 2556–2561 (2003)
Larsson, M. C. et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703–714 (2004)
Gray, J. M. et al. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430, 317–322 (2004)
Wingrove, J. A. & O’Farrell, P. H. Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98, 105–114 (1999)
Verma, A., Hirsch, D. J., Glatt, C. E., Ronnett, G. V. & Snyder, S. H. Carbon monoxide: a putative neural messenger. Science 259, 381–384 (1993)
Reinking, J. et al. The Drosophila nuclear receptor e75 contains heme and is gas responsive. Cell 122, 195–207 (2005)
Hou, S. et al. Myoglobin-like aerotaxis transducers in Archaea and Bacteria. Nature 403, 540–544 (2000)
Laissue, P. P. et al. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J. Comp. Neurol. 405, 543–552 (1999)
Fishilevich, E. et al. Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr. Biol. 15, 2086–2096 (2005)
Acknowledgements
We thank P. Howell and M. Q. Benedict of the CDC and MR4 for providing us with mosquitoes contributed by W. E. Collins; K. Kay and K. Fishilevich for technical assistance; and R. Axel, C. Bargmann, K. J. Lee and members of the Vosshall Laboratory for comments on the manuscript. This work was funded in part by a grant to R. Axel and L.B.V. from the Foundation for the National Institutes of Health through the Grand Challenges in Global Health Initiative and by an NIH grant to L.B.V. Support was contributed to W.D.J. from an NIH MSTP grant, to P.C. from the Jane Coffin Childs Memorial Fund for Medical Research and to I.G.K. from the Human Frontier Science Program.
Author Contributions W.D.J. carried out all the experiments and analysed the data. P.C. and I.G.K. generated and characterized the Gr63a-sytRFP transgene in the laboratory of S. L. Zipursky at UCLA. W.D.J. and L.B.V. together designed the experiments, interpreted the results, produced the figures, and wrote the paper.
Genbank accession numbers for A. gambiae genes in this paper are: GPROR7 (AY843205), GPRGR22 (DQ989011) and GPRGR24 (DQ989013). Genbank accession numbers for D. melanogaster genes in this paper are: Gr10a (DQ989010), Gr21a (DQ989014) and Gr63a (DQ989012).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
Genbank accession numbers for A. gambiae genes in this paper are: GPROR7 (AY843205), GPRGR22 (DQ989011) and GPRGR24 (DQ989013). Genbank accession numbers for D. melanogaster genes in this paper are: Gr10a (DQ989010), Gr21a (DQ989014) and Gr63a (DQ989012). Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.
Supplementary information
Supplementary Information
This file contains detailed Supplementary Methods. (PDF 112 kb)
Rights and permissions
About this article
Cite this article
Jones, W., Cayirlioglu, P., Grunwald Kadow, I. et al. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445, 86–90 (2007). https://doi.org/10.1038/nature05466
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature05466
This article is cited by
-
Stage- and sex-specific transcriptome analyses reveal distinctive sensory gene expression patterns in a butterfly
BMC Genomics (2021)
-
Insects locomotion, piercing, sucking and stinging mechanisms
Microsystem Technologies (2018)
-
Chemosensory genes in the antennal transcriptome of two syrphid species, Episyrphus balteatus and Eupeodes corollae (Diptera: Syrphidae)
BMC Genomics (2017)
-
Nepenthes pitchers are CO2-enriched cavities, emit CO2 to attract preys
Scientific Reports (2017)
-
Antennal transcriptome and expression analyses of olfactory genes in the sweetpotato weevil Cylas formicarius
Scientific Reports (2017)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.