Hold your breath – Differential behavioral and sensory acuity of mosquitoes to acetone and carbon dioxide

English version

Autoři: Majid Ghaninia ^aff001; Shahid Majeed ^aff003; Teun Dekker ^aff003; Sharon R. Hill ^aff003; Rickard Ignell ^aff003
Působiště autorů: School of Life Sciences, Arizona State University, Tempe, AZ, United States of America ^aff001; Division of Entomology, Department of Plant Protection, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran ^aff002; Disease Vector Group, Unit of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Alnarp, Sweden ^aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226815

Souhrn

Host seeking in the yellow fever mosquito, Aedes aegypti, and the African malaria mosquito, Anopheles coluzzii, relies on specific and generic host-derived odorants. Previous analyses indicate that the behavioral response of these species depends differentially on the presence of carbon dioxide (CO₂) and other constituents in human breath for activation and attraction. In this study, we use a flight tube assay and electrophysiological analysis to assess the role of acetone, a major component of exhaled human breath, in modulating the behavioral and sensory neuronal response of these mosquito species, in the presence and absence of CO₂. When presented alone at ecologically relevant concentrations, acetone increases attraction in Ae. aegypti, but not in An. coluzzii. Moreover, in combination with CO₂, human breath-equivalents of acetone ranging between 0.1 and 10 ppm reproduces a behavioral response similar to that observed to human breath in host-seeking Ae. aegypti, but not in An. coluzzii. Acetone does, however, reduce attraction to CO₂ in An. coluzzii, when presented at a higher concentration of 10 ppm. We identify the capitate peg A neuron of the maxillary palp of both species as a dual detector of CO₂ and acetone. The sensory response to acetone, or binary blends of acetone and CO₂, reflects the observed behavioral output in both Ae. aegypti and An. coluzzii. We conclude that host recognition is contextual and dependent on a combination of ecologically relevant odorants at naturally occurring concentrations that are encoded, in this case, by differences in the temporal structure of the neuronal response. This information should be considered when designing synthetic blends for that optimally attract mosquitoes for monitoring and control.

Klíčová slova:

Acetones – Aedes aegypti – Animal behavior – Behavior – Carbon dioxide – Mosquitoes – Neurons – Sensory neurons

Zdroje

1. Takken W, Verhulst NO. Host preferences of blood-feeding mosquitoes. Annual Review of Entomology. 2013;58:433–53. doi: 10.1146/annurev-ento-120811-153618 23020619

2. Potter CJ. Stop the biting: targeting a mosquito’s sense of smell. Cell. 2014;156(5):878–81. doi: 10.1016/j.cell.2014.02.003 24581489

3. Cardé RT. Multi-cue integration: how female mosquitoes locate a human host. Current Biology. 2015;25(18):R793–R5. doi: 10.1016/j.cub.2015.07.057 26394099

4. Majeed S, Hill SR, Birgersson G, Ignell R. Detection and perception of generic host volatiles by mosquitoes modulate host preference: context dependence of (R)-1-octen-3-ol. Royal Society Open Science. 2016;3(11):160467. doi: 10.1098/rsos.160467 28018630

5. Majeed S, Hill SR, Dekker T, Ignell R. Detection and perception of generic host volatiles by mosquitoes: responses to CO2 constrains host-seeking behaviour. Royal Society Open Science. 2017;4(5):170189. doi: 10.1098/rsos.170189 28573028

6. Okumu FO, Killeen GF, Ogoma S, Biswaro L, Smallegange RC, Mbeyela E, et al. Development and field evaluation of a synthetic mosquito lure that is more attractive than humans. PloS One. 2010;5(1):e8951. doi: 10.1371/journal.pone.0008951 20126628

7. Bruce TJ, Pickett JA. Perception of plant volatile blends by herbivorous insects–finding the right mix. Phytochemistry. 2011;72(13):1605–11. doi: 10.1016/j.phytochem.2011.04.011 21596403

8. Lu T, Qiu YT, Wang G, Kwon JY, Rutzler M, Kwon H-W, et al. Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Current Biology. 2007;17(18):1533–44. doi: 10.1016/j.cub.2007.07.062 17764944

9. Syed Z, Leal WS. Maxillary palps are broad spectrum odorant detectors in Culex quinquefasciatus. Chemical Senses. 2007;32(8):727–38. doi: 10.1093/chemse/bjm040 17569743

10. Dobbelaar P, Mottram T, Nyabadza C, Hobbs P, Elliott-Martin R, Schukken Y. Detection of ketosis in dairy cows by analysis of exhaled breath. Veterinary Quarterly. 1996;18(4):151–2. 8972064

11. Elliott-Martin R, Mottram T, Gardner J, Hobbs P, Bartlett P. Preliminary investigation of breath sampling as a monitor of health in dairy cattle. Journal of Agricultural Engineering Research. 1997;67(4):267–75.

12. Fenske JD, Paulson SE. Human breath emissions of VOCs. Journal of the Air & Waste Management Association. 1999;49(5):594–8.

13. Wahl HG, Hoffmann A, Luft D, Liebich HM. Analysis of volatile organic compounds in human urine by headspace gas chromatography–mass spectrometry with a multipurpose sampler. Journal of Chromatography A. 1999;847(1–2):117–25. doi: 10.1016/s0021-9673(99)00017-5 10431355

14. Knodt C, Shaw J, White G. Studies on ketosis in dairy cattle. I. Effect of stall and pasture feeding upon the concentration of blood and urinary acetone bodies of dairy cattle1. Journal of Dairy Science. 1942;25(10):837–49.

15. Vale G, Hall D. The role of 1-octen-3-ol, acetone and carbon dioxide in the attraction of tsetse flies, Glossina spp. (Diptera: Glossinidae), to ox odour. Bulletin of Entomological Research. 1985;75(2):209–18.

16. Torr S, Hall D, Smith J. Responses of tsetse flies (Diptera: Glossinidae) to natural and synthetic ox odours. Bulletin of Entomological Research. 1995;85(1):157–66.

17. Qiu Y, Smallegange R, Van Loon J, Takken W. Behavioural responses of Anopheles gambiae sensu stricto to components of human breath, sweat and urine depend on mixture composition and concentration. Medical and Veterinary Entomology. 2011;25(3):247–55. doi: 10.1111/j.1365-2915.2010.00924.x 21108650

18. Healy T, Copland M. Activation of Anopheles gambiae mosquitoes by carbon dioxide and human breath. Medical and Veterinary Entomology. 1995;9(3):331–6. doi: 10.1111/j.1365-2915.1995.tb00143.x 7548953

19. Takken W, Dekker T, Wijnholds Y. Odor-mediated flight behavior of Anopheles gambiae giles Sensu Stricto and An. stephensi liston in response to CO 2, acetone, and 1-octen-3-ol (Diptera: Culicidae). Journal of Insect Behavior. 1997;10(3):395–407.

20. Venkatesh P, Sen A. Laboratory evaluation of synthetic blends of l-(+)-lactic acid, ammonia, and ketones as potential attractants for Aedes aegypti. Journal of the American Mosquito Control Association. 2017;33(4):301–8. doi: 10.2987/16-6599.1 29369028

21. Bernier UR, Kline DL, Posey KH, Booth MM, Yost RA, Barnard DR. Synergistic attraction of Aedes aegypti (L.) to binary blends of L-lactic acid and acetone, dichloromethane, or dimethyl disulfide. Journal of Medical Entomology. 2003;40(5):653–6. doi: 10.1603/0022-2585-40.5.653 14596278

22. Bernier UR, Kline DL, Allan SA, Barnard DR. Laboratory comparison of Aedes aegypti attraction to human odors and to synthetic human odor compounds and blends. Journal of the American Mosquito Control Association. 2007;23(3):288–93. doi: 10.2987/8756-971X(2007)23[288:LCOAAA]2.0.CO;2 17939508

23. Grant A, Aghajanian J, O'Connell R, Wigton B. Electrophysiological responses of receptor neurons in mosquito maxillary palp sensilla to carbon dioxide. Journal of Comparative Physiology A. 1995;177(4):389–96.

24. Majeed S, Hill SR, Ignell R. Impact of elevated CO2 background levels on the host-seeking behaviour of Aedes aegypti. Journal of Experimental Biology. 2014;217(4):598–604.

25. Mboera L, Knols B, Takken W, Della Torre A. The response of Anopheles gambiae sl and A. funestus (Diptera: Culicidae) to tents baited with human odour or carbon dioxide in Tanzania. Bulletin of Entomological Research. 1997;87(2):173–8.

26. Ghaninia M, Ignell R, Hansson BS. Functional classification and central nervous projections of olfactory receptor neurons housed in antennal trichoid sensilla of female yellow fever mosquitoes, Aedes aegypti. European Journal of Neuroscience. 2007;26(6):1611–23. doi: 10.1111/j.1460-9568.2007.05786.x 17880395

27. Jones M, Gubbins S, Cubbin C. Circadian flight activity in four sibling species of the Anopheles gambiae complex (Diptera, Culicidae). Bulletin of Entomological Research. 1974;64(2):241–6.

28. Yee WL, Foster WA. Diel sugar-feeding and host-seeking rhythms in mosquitoes (Diptera: Culicidae) under laboratory conditions. Journal of Medical Entomology. 1992;29(5):784–91. doi: 10.1093/jmedent/29.5.784 1357175

29. Ghaninia M. Olfaction in mosquitoes: Neuroanatomy and electrophysiology of the olfactory system [Doctoral dissertation]: Swedish University of Agricultural Sciences, SE.; 2007.

30. Ghaninia M, Larsson M, Hansson BS, Ignell R. Natural odor ligands for olfactory receptor neurons of the female mosquito Aedes aegypti: use of gas chromatography-linked single sensillum recordings. Journal of Experimental Biology. 2008;211(18):3020–7.

31. Qiu YT, Van Loon JJ, Takken W, Meijerink J, Smid HM. Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae. Chemical Senses. 2006;31(9):845–63. doi: 10.1093/chemse/bjl027 16963500

32. Suer RA. Unravelling the malaria mosquito's sense of smell: neural and behavioural responses to human-derived compounds [Doctoral dissertation]: Wageningen University, NL.; 2011.

33. Khan A, Maibach HI. Effect of human breath on mosquito attraction to man. Mosquito News. 1972;32(1):11–5.

34. Turner SL, Li N, Guda T, Githure J, Cardé RT, Ray A. Ultra-prolonged activation of CO 2-sensing neurons disorients mosquitoes. Nature. 2011;474(7349):87. doi: 10.1038/nature10081 21637258

35. Tauxe GM, MacWilliam D, Boyle SM, Guda T, Ray A. Targeting a dual detector of skin and CO2 to modify mosquito host seeking. Cell. 2013;155(6):1365–79. doi: 10.1016/j.cell.2013.11.013 24315103

36. Coutinho-Abreu IV, Sharma K, Cui L, Yan G, Ray A. Odorant ligands for the CO 2 receptor in two Anopheles vectors of malaria. Scientific Reports. 2019;9(1):2549. doi: 10.1038/s41598-019-39099-0 30796292

37. MacWilliam D, Kowalewski J, Kumar A, Pontrello C, Ray A. Signaling mode of the broad-spectrum conserved CO2 receptor is one of the important determinants of odor valence in Drosophila. Neuron. 2018;97(5):1153–67. e4. doi: 10.1016/j.neuron.2018.01.028 29429938

38. Erdelyan C, Mahood T, Bader T, Whyard S. Functional validation of the carbon dioxide receptor genes in Aedes aegypti mosquitoes using RNA interference. Insect Molecular Biology. 2012;21(1):119–27. doi: 10.1111/j.1365-2583.2011.01120.x 22122783

39. McMeniman CJ, Corfas RA, Matthews BJ, Ritchie SA, Vosshall LB. Multimodal integration of carbon dioxide and other sensory cues drives mosquito attraction to humans. Cell. 2014;156(5):1060–71. doi: 10.1016/j.cell.2013.12.044 24581501

40. Smallegange RC, Takken W. Host-seeking behaviour of mosquitoes: responses to olfactory stimuli in the laboratory. Olfaction in vector-host interactions: Wageningen Academic Publishers; 2010. p. 143–80.

41. Takken W, Knols BG. Odor-mediated behavior of Afrotropical malaria mosquitoes. Annual Review of Entomology. 1999;44(1):131–57.

42. Mukabana WR, Takken W, Coe R, Knols BG. Host-specific cues cause differential attractiveness of Kenyan men to the African malaria vector Anopheles gambiae. Malaria Journal. 2002;1(1):17.

43. Smallegange RC, Bukovinszkiné-Kiss G, Otieno B, Mbadi PA, Takken W, Mukabana WR, et al. Identification of candidate volatiles that affect the behavioural response of the malaria mosquito Anopheles gambiae sensu stricto to an active kairomone blend: laboratory and semi‐field assays. Physiological Entomology. 2012;37(1):60–71.

44. Omondi A, Ghaninia M, Dawit M, Svensson T, Ignell R. Age-dependent regulation of host seeking in Anopheles coluzzii. Scientific Reports. 2019;9(1):9699. doi: 10.1038/s41598-019-46220-w 31273284

45. Geier M, Bosch OJ, Boeckh J. Influence of odour plume structure on upwind flight of mosquitoes towards hosts. Journal of Experimental Biology. 1999;202(12):1639–48.

46. Smallegange RC, Qiu YT, Bukovinszkiné-Kiss G, Van Loon JJ, Takken W. The effect of aliphatic carboxylic acids on olfaction-based host-seeking of the malaria mosquito Anopheles gambiae sensu stricto. Journal of Chemical Ecology. 2009;35(8):933. doi: 10.1007/s10886-009-9668-7 19626371

47. Smallegange RC, Qiu YT, van Loon JJ, Takken W. Synergism between ammonia, lactic acid and carboxylic acids as kairomones in the host-seeking behaviour of the malaria mosquito Anopheles gambiae sensu stricto (Diptera: Culicidae). Chemical Senses. 2005;30(2):145–52. doi: 10.1093/chemse/bji010 15703334

48. Verhulst NO, Mukabana WR, Takken W, Smallegange RC. Human skin microbiota and their volatiles as odour baits for the malaria mosquito Anopheles gambiae ss. Entomologia Experimentalis et Applicata. 2011;139(2):170–9.

49. Dekker T, Geier M, Cardé RT. Carbon dioxide instantly sensitizes female yellow fever mosquitoes to human skin odours. Journal of Experimental Biology. 2005;208(15):2963–72.

Hold your breath – Differential behavioral and sensory acuity of mosquitoes to acetone and carbon dioxide

Souhrn

Klíčová slova:

Zdroje

PLOS One

Svět praktické medicíny 1/2024 (znalostní test z časopisu)

Koncepce osteologické péče pro gynekology a praktické lékaře

Sekvenční léčba schizofrenie

Hypertenze a hypercholesterolémie – synergický efekt léčby

Význam metforminu pro „udržitelnou“ terapii diabetu