Identification of human skin bacteria attractive to the Asian Tiger mosquito.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
12 2019
12 2019
Historique:
received:
29
03
2019
revised:
26
08
2019
accepted:
27
08
2019
pubmed:
30
8
2019
medline:
12
5
2020
entrez:
30
8
2019
Statut:
ppublish
Résumé
Aedes albopictus is a vector of arboviruses and filarial nematodes. Originating from Asia, this mosquito has rapidly expanded its geographical distribution and colonized areas across both temperate and tropical regions. Due to the increase in insecticide resistance, the use of environmentally friendly vector control methods is encouraged worldwide. Using methods based on semiochemicals in baited traps are promising for management of mosquito populations. Interestingly, human skin microbiota was shown to generate volatile compounds that attract the mosquito species Anopheles gambiae and Aedes aegypti. Here, we investigated the composition of skin bacteria from different volunteers and the attractive potential of individual isolates to nulliparous Ae. albopictus females. We showed that three out of 16 tested isolates were more attractive and two were more repulsive. We identified dodecenol as being preferentially produced by attractive isolates and 2-methyl-1-butanol (and to a lesser extent 3-methyl-1-butanol) as being overproduced by these isolates compared with the other ones. Those bacterial volatile organic compounds represent promising candidates but further studies are needed to evaluate their potential application for baited traps improvement.
Identifiants
pubmed: 31464044
doi: 10.1111/1462-2920.14793
doi:
Substances chimiques
Volatile Organic Compounds
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4662-4674Subventions
Organisme : French National Research Program for Environmental and Occupational Health of ANSES
ID : 2014/1/020
Pays : International
Organisme : University of Lyon in the frame of the Programme Invetissement d'Avenir
ID : ANR-16-IDEX-0005
Pays : International
Informations de copyright
© 2019 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Andrianjafy, T.M., Ravaomanarivo, L.H., Ramanandraibe, V.V., Rakotondramanga, M.F., Mavingui, P., and Lemaire, M. (2018) Synthesis, bioassays and field evaluation of hydroxycoumarins and their alkyl derivatives as repellents or kairomones for Aedes albopictus Skuse (Diptera: Culicidae). J Chem Ecol 44: 299-311.
Bawdon, D., Cox, D.S., Ashford, D., James, A.G., and Thomas, G.H. (2015) Identification of axillary Staphylococcus sp. involved in the production of the malodorous thioalcohol 3-methyl-3-sufanylhexan-1-ol. FEMS Microbiol Lett 362: fnv111.
Bernier, U.R., Kline, D.L., Barnard, D.R., Schreck, C.E., and Yost, R.A. (2000) 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.
Bohbot, J.D., and Dickens, J.C. (2010) Insect repellents: modulators of mosquito odorant receptor activity. PLoS One 5: e12138.
Bonizzoni, M., Gasperi, G., Chen, X., and James, A.A. (2013) The invasive mosquito species Aedes albopictus: current knowledge and future perspectives. Trends Parasitol 29: 460-468.
Braks, M.A.H., and Takken, W. (1999) Incubated human sweat but not fresh sweat attracts the malaria mosquito Anopheles gambiae sensu stricto. J Chem Ecol 25: 663-672.
Chen, Q., Man, Y., Li, J., Pei, D., and Wu, W. (2017) Olfactory ionotropic receptors in mosquitoes Aedes albopictus (Diptera:Culucidae). J Med Entomol 54: 1229-1235.
Delatte, H., Desvars, A., Bouétard, A., Bord, S., Gimonneau, G., Vourc'h, G., and Fontenille, D. (2010) Blood-feeding behavior of Aedes albopictus, a vector of Chikungunya on La Réunion. Vector Borne Zoonotic Dis 10: 249-258.
Frei, J., Kröber, T., Troccaz, M., Starkenmann, C., and Guerin, P.M. (2017) Behavioral response of the malaria mosquito, Anopheles gambiae, to human sweat inoculated with axilla bacteria and to volatiles composing human axillary odor. Chem Senses 42: 121-131.
Goubert, C., Minard, G., Vieira, C., and Boulesteix, M. (2016) Population genetics of the Asian tiger mosquito Aedes albopictus, an invasive vector of human diseases. Heredity 117: 125-134.
Grice, E.A., Kong, H.H., Conlan, S., Deming, C.B., Davis, J., Young, A.C., et al. (2009) Topographical and temporal diversity of the human skin microbiome. Science 324: 1190-1192.
Guha, L., Seenivasagan, T., Iqbal, S.T., Agrawal, O.P., and Parashar, B.D. (2014) Behavioral and electrophysiological responses of Aedes albopictus to certain acids and alcohols present in human skin emanations. Parasitol Res 113: 3781-3787.
Homan, T., Hiscox, A., Mweresa, C.K., Masiga, D., Mukabana, W.R., Oria, P., et al. (2016) The effect of mass mosquito trapping on malaria transmission and disease burden (SolarMal): a stepped-wedge cluster-randomised trial. Lancet 388: 1193-1201.
Huber-Carol, C., Balakrishnan, N., Nikulin, M.S., and Mesbah, M. (eds). (2002) Goodness-of-Fit Tests and Model Validity. Basel, Switzerland: Birkhäuser.
James, A.G., Hyliands, D., and Johnston, H. (2004) Generation of volatile fatty acids by axillary bacteria. Int J Cosmet Sci 26: 149-156.
Maibach, H.I., Skinner, W.A., Strauss, W.G., and Khan, A.A. (1966) Factors that attract and repel mosquitoes in human skin. JAMA 196: 263-266.
Majeed, S., Hill, S.R., Birgersson, G., and Ignell, R. (2016) Detection and perception of generic host volatiles by mosquitoes modulate host preference: context dependence of (R)-1-octen-3-ol. R Soc Open Sci 3: 160467.
Mathew, N., Ayyanar, E., Shanmugavelu, S., and Muthuswamy, K. (2013) Mosquito attractant blends to trap host seeking Aedes aegypti. Parasitol Res 112: 1305-1312.
McBride, C.S., Baier, F., Omondi, A.B., Spitzer, S.A., Lutomiah, J., Sang, R., et al. (2014) Evolution of mosquito preference for humans linked to an odorant receptor. Nature 515: 222-227.
McDonald, J.H. (2014) Handbook of Biological Statistics, 3rd ed. Baltimore, MD: Sparky House Publishing.
Mukabana, W.R., Mweresa, C.K., Otieno, B., Omusula, P., Smallegange, R.C., van Loon, J.J., and Takken, W. (2012) A novel synthetic odorant blend for trapping of malaria and other African mosquito species. J Chem Ecol 38: 235-244.
Mweresa, C.K., Omusula, P., Otieno, B., van Loon, J.J., Takken, W., and Mukabana, W.R. (2014) Molasses as a source of carbon dioxide for attracting the malaria mosquitoes Anopheles gambiae and Anopheles funestus. Malar J 13: 160.
Nicolaides, N. (1974) Skin lipids: their biochemical uniqueness. Unlike internal organs, the skin biosynthesizes and excretes unusual fat soluble substance. Science 186: 19-26.
Paixão, E.S., Teixeira, M.G., and Rodrigues, L.C. (2018) Zika, chikungunya and dengue: the causes and threats of new and re-emerging arboviral diseases. BMJ Glob Health 3: e000530.
Paupy, C., Delatte, H., Bagny, L., Corbel, V., and Fontenille, D. (2009) Aedes albopictus, an arbovirus vector: from the darkness to the light. Microbes Infect 11: 1177-1185.
Potter, C.J. (2014) Stop the biting: targeting a mosquito's sense of smell. Cell 156: 878-881.
Raji, J.I., and DeGennaro, M. (2017) Genetic analysis of mosquito detection of humans. Curr Opin Insect Sci 20: 34-38.
Raji, J.I., Melo, N., Castillo, J.S., Gonzalez, S., Saldana, V., Stensmyr, M.C., and DeGennaro, M. (2019) Aedes aegypti mosquitoes detect acidic volatiles found in human odor using the IR8a pathway. Curr Biol 29: 1253-1262.e7.
Ray, A. (2015) Reception of odors and repellents in mosquitoes. Curr Opin Neurobiol 34: 158-164.
Seenivasagan, T., Guha, L., Parashar, B.D., Agrawal, O.P., and Sukumaran, D. (2014) Olfaction in Asian tiger mosquito Aedes albopictus: flight orientation response to certain saturated carboxylic acids in human skin emanations. Parasitol Res 113: 1927-1932.
Smallegange, R.C., and Takken, W. (2010) Host-seeking behaviour of mosquitoes - responses to olfactory stimuli in the laboratory. In Olfaction in Vector-Host Interactions, Takken, W., and Knols, B.G.J. (eds). Netherlands: Wageningen Academic Publishers, pp. 143-180.
Smallegange, R.C., Verhulst, N.O., and Takken, W. (2011) Sweaty skin: an invitation to bite? Trends Parasitol 27: 143-148.
Sukuraman, D. (2016) A review on use of attractants and traps for host seeking Aedes aegypti mosquitoes. Indian J Nat Prod Resour 7: 207-214.
Takken, W., and Knols, B.G.J. (1999) Odor-mediated behavior of afrotropical malaria mosquitoes. Annu Rev Entomol 44: 131-157.
Takken, W., and Verhulst, N.O. (2017) Chemical signaling in mosquito-host interactions: the role of human skin microbiota. Curr Opin Insect Sci 20: 68-74.
Valiente Moro, C., Tran, F.H., Raharimalala, F.N., Ravelonandro, P., and Mavingui, P. (2013) Diversity of culturable bacteria including Pantoea in wild mosquito Aedes albopictus. BMC Microbiol 13: 70.
Verhulst, N.O., Andriessen, R., Groenhagen, U., Bukovinszkiné Kiss, G., Schulz, S., Takken, W., et al. (2010a) Differential attraction of malaria mosquitoes to volatile blends produced by human skin bacteria. PLoS One 5: e15829.
Verhulst, N.O., Beijleveld, H., Knols, B.G., Takken, W., Schraa, G., Bouwmeester, H.J., and Smallegange, R.C. (2009) Cultured skin microbiota attracts malaria mosquitoes. Malar J 8: 302.
Verhulst, N.O., Qiu, Y.T., Beijleveld, H., Maliepaard, C., Knights, D., Schulz, S., et al. (2011) Composition of human skin microbiota affects attractiveness to malaria mosquitoes. PLoS One 6: e28991.
Verhulst, N.O., Takken, W., Dicke, M., Schraa, G., and Smallegange, R.C. (2010b) Chemical ecology of interactions between human skin microbiota and mosquitoes. FEMS Microbiol Ecol 74: 1-9.