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Odorant reception in the malaria mosquito Anopheles gambiae


The mosquito Anopheles gambiae is the major vector of malaria in sub-Saharan Africa. It locates its human hosts primarily through olfaction, but little is known about the molecular basis of this process. Here we functionally characterize the Anopheles gambiae odorant receptor (AgOr) repertoire. We identify receptors that respond strongly to components of human odour and that may act in the process of human recognition. Some of these receptors are narrowly tuned, and some salient odorants elicit strong responses from only one or a few receptors, suggesting a central role for specific transmission channels in human host-seeking behaviour. This analysis of the Anopheles gambiae receptors permits a comparison with the corresponding Drosophila melanogaster odorant receptor repertoire. We find that odorants are differentially encoded by the two species in ways consistent with their ecological needs. Our analysis of the Anopheles gambiae repertoire identifies receptors that may be useful targets for controlling the transmission of malaria.

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Figure 1: Functional characterization of the AgOrs.
Figure 2: Tuning breadths of receptors.
Figure 3: Odorant tuning curves.
Figure 4: Distribution of responses across a physicochemical odour space.
Figure 5: Distribution of odorants in a receptor activity-based odour space.


  1. 1

    World Health Organization. World Malaria Report〉 (2008)

  2. 2

    Zwiebel, L. J. & Takken, W. Olfactory regulation of mosquito-host interactions. Insect Biochem. Mol. Biol. 34, 645–652 (2004)

    CAS  Article  Google Scholar 

  3. 3

    Takken, W. The role of olfaction in host-seeking of mosquitos: a review. Insect Sci. Applic. 12, 287–295 (1991)

    Google Scholar 

  4. 4

    Takken, W. & Knols, B. G. J. Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu. Rev. Entomol. 44, 131–157 (1999)

    CAS  Article  Google Scholar 

  5. 5

    Su, C. Y., Menuz, K. & Carlson, J. R. Olfactory perception: receptors, cells, and circuits. Cell 139, 45–59 (2009)

    CAS  Article  Google Scholar 

  6. 6

    Hill, C. A. et al. G protein coupled receptors in Anopheles gambiae . Science 298, 176–178 (2002)

    ADS  CAS  Article  Google Scholar 

  7. 7

    Fox, A. N., Pitts, R. J., Robertson, H. M., Carlson, J. R. & Zwiebel, L. J. Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding. Proc. Natl Acad. Sci. USA 98, 14693–14697 (2001)

    ADS  CAS  Article  Google Scholar 

  8. 8

    Hallem, E. A., Fox, A. N., Zwiebel, L. J. & Carlson, J. R. Olfaction: mosquito receptor for human-sweat odorant. Nature 427, 212–213 (2004)

    ADS  CAS  Article  Google Scholar 

  9. 9

    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)

    CAS  Article  Google Scholar 

  10. 10

    Kreher, S. A., Mathew, D., Kim, J. & Carlson, J. R. Translation of sensory input into behavioral output via an olfactory system. Neuron 59, 110–124 (2008)

    CAS  Article  Google Scholar 

  11. 11

    Hallem, E. A., Ho, M. G. & Carlson, J. R. The molecular basis of odor coding in the Drosophila antenna. Cell 117, 965–979 (2004)

    CAS  Article  Google Scholar 

  12. 12

    Hallem, E. A. & Carlson, J. R. Coding of odors by a receptor repertoire. Cell 125, 143–160 (2006)

    CAS  Article  Google Scholar 

  13. 13

    Gaunt, M. W. & Miles, M. A. An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Mol. Biol. Evol. 19, 748–761 (2002)

    CAS  Article  Google Scholar 

  14. 14

    Lu, T. et al. Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae . Curr. Biol. 17, 1533–1544 (2007)

    CAS  Article  Google Scholar 

  15. 15

    Malnic, B., Hirono, J., Sato, T. & Buck, L. B. Combinatorial receptor codes for odors. Cell 96, 713–723 (1999)

    CAS  Article  Google Scholar 

  16. 16

    Saito, H., Chi, Q., Zhuang, H., Matsunami, H. & Mainland, J. D. Odor coding by a mammalian receptor repertoire. Sci. Signal. 2, ra9 (2009)

    Article  Google Scholar 

  17. 17

    Wilson, R. I. & Mainen, Z. F. Early events in olfactory processing. Annu. Rev. Neurosci. 29, 163–201 (2006)

    CAS  Article  Google Scholar 

  18. 18

    Meijerink, J. et al. Identification of olfactory stimulants for Anopheles gambiae from human sweat samples. J. Chem. Ecol. 26, 1367–1382 (2000)

    CAS  Article  Google Scholar 

  19. 19

    Verhulst, N. O. et al. Cultured skin microbiota attracts malaria mosquitoes. Malar. J. 8, 302 (2009)

    Article  Google Scholar 

  20. 20

    Sun, H. et al. Alcohol, volatile fatty acid, phenol, and methane emissions from dairy cows and fresh manure. J. Environ. Qual. 37, 615–622 (2008)

    CAS  Article  Google Scholar 

  21. 21

    Gutiérrez-García, A. G., Contreras, C. M., Mendoza-Lopez, M. R., Garcia-Barradas, O. & Cruz-Sanchez, J. S. Urine from stressed rats increases immobility in receptor rats forced to swim: role of 2-heptanone. Physiol. Behav. 91, 166–172 (2007)

    Article  Google Scholar 

  22. 22

    TNO. Volatile Compounds in Food: Qualitative and Quantitative Data〉 (2004)

  23. 23

    Morton, I. D. & MacLeod, A. J. The Flavour Of Fruits (Elsevier Science, 1990)

    Google Scholar 

  24. 24

    Millar, J. G., Chaney, J. D. & Mulla, M. S. Identification of oviposition attractants for culex-quinquefasciatus from fermented bermuda grass infusions. J. Am. Mosq. Control Assoc. 8, 11–17 (1992)

    CAS  PubMed  Google Scholar 

  25. 25

    Syed, Z. & Leal, W. S. Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant. Proc. Natl Acad. Sci. USA 106, 18803–18808 (2009)

    ADS  CAS  Article  Google Scholar 

  26. 26

    Blackwell, A. & Johnson, S. N. Electrophysiological investigation of larval water and potential oviposition chemo-attractants for Anopheles gambiae s.s. Ann. Trop. Med. Parasitol. 94, 389–398 (2000)

    CAS  Article  Google Scholar 

  27. 27

    Lindh, J. M., Kannaste, A., Knols, B. G. J., Faye, I. & Borg-Karlson, A. K. Oviposition responses of Anopheles Gambiae s.s. (Diptera: Culicidae) and identification of volatiles from bacteria-containing solutions. J. Med. Entomol. 45, 1039–1049 (2008)

    CAS  Article  Google Scholar 

  28. 28

    Kostelc, J. G., Preti, G., Zelson, P. R., Stoller, N. H. & Tonzetich, J. Salivary volatiles as indicators of periodontitis. J. Periodontal Res. 15, 185–192 (1980)

    CAS  Article  Google Scholar 

  29. 29

    Moore, S. J. & Debboun, M. in Insect Repellents: Principles, Methods, and Uses (eds Debboun, M., Frances, S. P. & Strickman, D.) 3–30 (CRC, 2007)

    Google Scholar 

  30. 30

    Omolo, M. O., Okinyo, D., Ndiege, I. O., Lwande, W. & Hassanali, A. Repellency of essential oils of some Kenyan plants against Anopheles gambiae . Phytochemistry 65, 2797–2802 (2004)

    CAS  Article  Google Scholar 

  31. 31

    Tangerman, A., Meuwesearends, M. T. & Vantongeren, J. H. M. A new sensitive assay for measuring volatile sulfur-compounds in human breath by tenax trapping and gas-chromatography and its application in liver-cirrhosis. clin. Chim. Acta 130, 103–110 (1983)

    CAS  Article  Google Scholar 

  32. 32

    Allan, S. A., Bernier, U. R. & Kline, D. L. Evaluation of oviposition substrates and organic infusions on collection of Culex in Florida. J. Am. Mosq. Control Assoc. 21, 268–273 (2005)

    Article  Google Scholar 

  33. 33

    Haddad, R. et al. A metric for odorant comparison. Nature Methods 5, 425–429 (2008)

    CAS  Article  Google Scholar 

  34. 34

    Logan, J. G. et al. Identification of human-derived volatile chemicals that interfere with attraction of Aedes aegypti mosquitoes. J. Chem. Ecol. 34, 308–322 (2008)

    CAS  Article  Google Scholar 

  35. 35

    Curran, A. M., Ramirez, C. F., Schoon, A. A. & Furton, K. G. The frequency of occurrence and discriminatory power of compounds found in human scent across a population determined by SPME-GEMS. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 846, 86–97 (2007)

    CAS  Article  Google Scholar 

  36. 36

    Curran, A. M., Rabin, S. I., Prada, P. A. & Furton, K. G. Comparison of the volatile organic compounds present in human odor using SPME-GC/MS. J. Chem. Ecol. 31, 1607–1619 (2005)

    CAS  Article  Google Scholar 

  37. 37

    Cork, A. & Park, K. C. Identification of electrophysiologically-active compounds for the malaria mosquito, Anopheles gambiae, in human sweat extracts. Med. Vet. Entomol. 10, 269–276 (1996)

    CAS  Article  Google Scholar 

  38. 38

    Bernier, U. R., Kline, D. L., Schreck, C. E., Yost, R. A. & Barnard, D. R. Chemical analysis of human skin emanations: comparison of volatiles from humans that differ in attraction of Aedes aegypti (Diptera: Culicidae). J. Am. Mosq. Control Assoc. 18, 186–195 (2002)

    CAS  PubMed  Google Scholar 

  39. 39

    Bernier, U. R., Kline, D. L., Barnard, D. R., Schreck, C. E. & Yost, R. A. Analysis of human skin emanations by gas chromatography/mass spectrometry. 2. Identification of volatile compounds that are candidate attractants for the yellow fever mosquito (Aedes aegypti). Anal. Chem. 72, 747–756 (2000)

    CAS  Article  Google Scholar 

  40. 40

    Gallagher, M. et al. Analyses of volatile organic compounds from human skin. Br. J. Dermatol. 159, 780–791 (2008)

    CAS  Article  Google Scholar 

  41. 41

    Kreher, S. A., Kwon, J. Y. & Carlson, J. R. The molecular basis of odor coding in the Drosophila larva. Neuron 46, 445–456 (2005)

    CAS  Article  Google Scholar 

  42. 42

    Benton, R., Vannice, K. S., Gomez-Diaz, C. & Vosshall, L. B. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila . Cell 136, 149–162 (2009)

    CAS  Article  Google Scholar 

  43. 43

    Olsen, S. R. & Wilson, R. I. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452, 956–960 (2008)

    ADS  CAS  Article  Google Scholar 

  44. 44

    Schlief, M. L. & Wilson, R. I. Olfactory processing and behavior downstream from highly selective receptor neurons. Nature Neurosci. 10, 623–630 (2007)

    CAS  Article  Google Scholar 

  45. 45

    Yao, C. A., Ignell, R. & Carlson, J. R. Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J. Neurosci. 25, 8359–8367 (2005)

    CAS  Article  Google Scholar 

  46. 46

    Larsson, M. C. et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703–714 (2004)

    CAS  Article  Google Scholar 

  47. 47

    Xia, Y. et al. The molecular and cellular basis of olfactory-driven behavior in Anopheles gambiae larvae. Proc. Natl Acad. Sci. USA 105, 6433–6438 (2008)

    ADS  CAS  Article  Google Scholar 

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We thank W. van der Goes van Naters and C. Yao for help with electrophysiology, E. Hallem, S. Kreher, J. Salzman and T. Emonet for assistance with data analyses, and T.-W. Koh for comments on the manuscript. We thank P. Graham, Z. Berman, A. Rabin, M. Dillon and E. Kelley-Swift for technical assistance. We thank Y.-T. Qiu for assistance in generating Fig. 1b and Supplementary Fig. 1. This work was funded in part by grants from the Foundation for the National Institutes of Health (NIH) through the Grand Challenges in Global Health Initiative to L.J.Z., and from the NIH to L.J.Z. and J.R.C. A.F.C. is supported by an NIH Medical Scientist Training Program grant (2T32GM07205).

Author Contributions Electrophysiology and computational analysis were performed by A.F.C. Molecular cloning was performed by A.F.C., G.W. and C.-Y.S. A.F.C. and J.R.C. wrote the manuscript. All authors contributed to the design and interpretation of the study.

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Correspondence to John R. Carlson.

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The authors declare no competing financial interests.

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Supplementary Information

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Carey, A., Wang, G., Su, CY. et al. Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464, 66–71 (2010).

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