Odor-mediated response of gravid Aedes aegypti to mosquito-associated symbiotic bacteria.

Complex oviposition decisions allow gravid Aedes aegypti mosquitoes to select suitable sites for egg-laying to increase the probability that their progeny will thrive. The bacterial communities present in larval niches influence mosquito oviposition behavior, and gravid mosquitoes transmit key microbial associates to breeding sites during oviposition. Our study evaluated whether symbiotic Klebsiella sp., which are strongly associated with mosquitoes, emit volatiles that affect mosquito oviposition decisions. Dual-choice behavioral assays demonstrated that volatile organic compounds emitted by Klebsiella sp. induce a preference in oviposition decisions by Ae. aegypti. Bacterial headspace volatiles were sampled by solid-phase microextraction, and subsequent combined gas chromatography and electroantennogram detection analysis, revealed that the antennae of gravid females detect two compounds present in the Klebsiella sp. headspace. These compounds were identified by gas chromatography and mass spectrometry as 2-ethyl hexanol and 2,4-di-tert-butylphenol. The binary blend of these compounds elicited a dose-dependent egg-laying preference by gravid mosquitoes. We propose that bacterial symbionts, which are associated with gravid mosquitoes and may be transferred to aquatic habitats during egg-laying, together with their volatiles act as oviposition cues indicating the suitability of active breeding sites to conspecific females.

[1]  F. Tripet,et al.  Standardised bioassays reveal that mosquitoes learn to avoid compounds used in chemical vector control after a single sub-lethal exposure , 2022, Scientific Reports.

[2]  M. Lorenzo,et al.  Multi-Omic Analysis of Symbiotic Bacteria Associated With Aedes aegypti Breeding Sites , 2021, Frontiers in Microbiology.

[3]  S. Tanamas,et al.  Effectiveness of Wolbachia-infected mosquito deployments in reducing the incidence of dengue and other Aedes-borne diseases in Niterói, Brazil: A quasi-experimental study , 2021, PLoS neglected tropical diseases.

[4]  E. Desouhant,et al.  Microorganisms Associated with Mosquito Oviposition Sites: Implications for Habitat Selection and Insect Life Histories , 2021, Microorganisms.

[5]  P. Ryan,et al.  Large-Scale Deployment and Establishment of Wolbachia Into the Aedes aegypti Population in Rio de Janeiro, Brazil , 2021, bioRxiv.

[6]  F. Scolari,et al.  Exploring Changes in the Microbiota of Aedes albopictus: Comparison Among Breeding Site Water, Larvae, and Adults , 2021, Frontiers in Microbiology.

[7]  W. Tadei,et al.  Culturable bacteria associated with Anopheles darlingi and their paratransgenesis potential , 2021, Malaria journal.

[8]  W. Takken,et al.  Synergism between nonane and emanations from soil as cues in oviposition‐site selection of natural populations of Anopheles gambiae and Culex quinquefasciatus , 2020, Malaria journal.

[9]  S. Hapfelmeier,et al.  Production of germ-free mosquitoes via transient colonisation allows stage-specific investigation of host–microbiota interactions , 2019, Nature Communications.

[10]  W. Takken,et al.  Exploiting the chemical ecology of mosquito oviposition behavior in mosquito surveillance and control: a review , 2020, Journal of Vector Ecology.

[11]  I. Velez,et al.  Description of the ovarian microbiota of Aedes aegypti (L) Rockefeller strain. , 2020, Acta tropica.

[12]  B. Hassan,et al.  Vertically Transmitted Gut Bacteria and Nutrition Influence the Immunity and Fitness of Bactrocera dorsalis Larvae , 2020, Frontiers in Microbiology.

[13]  T. Fukatsu,et al.  Relevance of microbial symbiosis to insect behavior. , 2020, Current opinion in insect science.

[14]  Shiyou Li,et al.  Natural Sources and Bioactivities of 2,4-Di-Tert-Butylphenol and Its Analogs , 2020, Toxins.

[15]  G. Wolff,et al.  Geosmin Attracts Aedes aegypti Mosquitoes to Oviposition Sites , 2019, Current Biology.

[16]  M. Jacobs-Lorena,et al.  Mosquito Microbiota and Implications for Disease Control. , 2019, Trends in parasitology.

[17]  D. Weetman,et al.  Management of insecticide resistance in the major Aedes vectors of arboviruses: Advances and challenges , 2019, PLoS neglected tropical diseases.

[18]  F. Scolari,et al.  Aedes spp. and Their Microbiota: A Review , 2019, Front. Microbiol..

[19]  Guofa Zhou,et al.  Bacterial microbiota assemblage in Aedes albopictus mosquitoes and its impacts on larval development , 2018, Molecular ecology.

[20]  C. Valiente Moro,et al.  The mosquito holobiont: fresh insight into mosquito-microbiota interactions , 2018, Microbiome.

[21]  Stevenn Volant,et al.  Carryover effects of larval exposure to different environmental bacteria drive adult trait variation in a mosquito vector , 2017, Science Advances.

[22]  M. Alejandra,et al.  Culex pipiens Development Is Greatly Influenced by Native Bacteria and Exogenous Yeast , 2016, PloS one.

[23]  V. Veer,et al.  Molecular characterization of midgut microbiota of Aedes albopictus and Aedes aegypti from Arunachal Pradesh, India , 2015, Parasites & Vectors.

[24]  C. Arellano,et al.  Oviposition responses of Aedes mosquitoes to bacterial isolates from attractive bamboo infusions , 2015, Parasites & Vectors.

[25]  H. Overgaard,et al.  Comparative assessment of the bacterial communities associated with Aedes aegypti larvae and water from domestic water storage containers , 2014, Parasites & Vectors.

[26]  B. D. Parashar,et al.  Midgut Microbial Community of Culex quinquefasciatus Mosquito Populations from India , 2013, PloS one.

[27]  A. James,et al.  orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET , 2013, Nature.

[28]  P. Rossi,et al.  Mosquito/microbiota interactions: from complex relationships to biotechnological perspectives. , 2012, Current opinion in microbiology.

[29]  M. A. Berbert-Molina,et al.  Culture-dependent and culture-independent characterization of microorganisms associated with Aedes aegypti (Diptera: Culicidae) (L.) and dynamics of bacterial colonization in the midgut. , 2010, Acta tropica.

[30]  N. Peabody,et al.  Establishment and Vertical Passage of Enterobacter (Pantoea) Agglomerans and Klebsiella pneumoniae through All Life Stages of the Mediterranean Fruit Fly (Diptera: Tephritidae) , 2009 .

[31]  B. Knols,et al.  Oviposition Responses of Anopheles gambiae s.s. (Diptera: Culicidae) and Identification of Volatiles from Bacteria-Containing Solutions , 2008, Journal of medical entomology.

[32]  Coby Schal,et al.  Identification of bacteria and bacteria-associated chemical cues that mediate oviposition site preferences by Aedes aegypti , 2008, Proceedings of the National Academy of Sciences.

[33]  B. Knols,et al.  Mediation of oviposition site selection in the African malaria mosquito Anopheles gambiae (Diptera: Culicidae) by semiochemicals of microbial origin , 2004 .