Establishment of a Wolbachia superinfection in Aedes aegypti mosquitoes as a potential approach for future resistance management

D Albert Joubert, Thomas Walker, Lauren B Carrington, Jyotika Taneja De Bruyne, Duong Hue T Kien, Nhat Le Thanh Hoang, Nguyen Van Vinh Chau, Inaki Iturbe-Ormaetxe, Cameron P Simmons, Scott L O'Neill

Research output: Contribution to journalArticleResearchpeer-review

76 Citations (Scopus)

Abstract

Wolbachia pipientis is an endosymbiotic bacterium estimated to chronically infect between 40–75% of all arthropod species. Aedes aegypti, the principle mosquito vector of dengue virus (DENV), is not a natural host of Wolbachia. The transinfection of Wolbachia strains such as wAlbB, wMel and wMelPop-CLA into Ae. aegypti has been shown to significantly reduce the vector competence of this mosquito for a range of human pathogens in the laboratory. This has led to wMel-transinfected Ae. aegypti currently being released in five countries to evaluate its effectiveness to control dengue disease in human populations. Here we describe the generation of a superinfected Ae. aegypti mosquito line simultaneously infected with two avirulent Wolbachia strains, wMel and wAlbB. The line carries a high overall Wolbachia density and tissue localisation of the individual strains is very similar to each respective single infected parental line. The superinfected line induces unidirectional cytoplasmic incompatibility (CI) when crossed to each single infected parental line, suggesting that the superinfection would have the capacity to replace either of the single constituent infections already present in a mosquito population. No significant differences in fitness parameters were observed between the superinfected line and the parental lines under the experimental conditions tested. Finally, the superinfected line blocks DENV replication more efficiently than the single wMel strain when challenged with blood meals from viremic dengue patients. These results suggest that the deployment of superinfections could be used to replace single infections and may represent an effective strategy to help manage potential resistance by DENV to field deployments of single infected strains.
Original languageEnglish
Pages (from-to)1-19
Number of pages19
JournalPLoS Pathogens
Volume12
Issue number2
DOIs
Publication statusPublished - 2016

Cite this

Joubert, D Albert ; Walker, Thomas ; Carrington, Lauren B ; Taneja De Bruyne, Jyotika ; Kien, Duong Hue T ; Le Thanh Hoang, Nhat ; Chau, Nguyen Van Vinh ; Iturbe-Ormaetxe, Inaki ; Simmons, Cameron P ; O'Neill, Scott L. / Establishment of a Wolbachia superinfection in Aedes aegypti mosquitoes as a potential approach for future resistance management. In: PLoS Pathogens. 2016 ; Vol. 12, No. 2. pp. 1-19.
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title = "Establishment of a Wolbachia superinfection in Aedes aegypti mosquitoes as a potential approach for future resistance management",
abstract = "Wolbachia pipientis is an endosymbiotic bacterium estimated to chronically infect between 40–75{\%} of all arthropod species. Aedes aegypti, the principle mosquito vector of dengue virus (DENV), is not a natural host of Wolbachia. The transinfection of Wolbachia strains such as wAlbB, wMel and wMelPop-CLA into Ae. aegypti has been shown to significantly reduce the vector competence of this mosquito for a range of human pathogens in the laboratory. This has led to wMel-transinfected Ae. aegypti currently being released in five countries to evaluate its effectiveness to control dengue disease in human populations. Here we describe the generation of a superinfected Ae. aegypti mosquito line simultaneously infected with two avirulent Wolbachia strains, wMel and wAlbB. The line carries a high overall Wolbachia density and tissue localisation of the individual strains is very similar to each respective single infected parental line. The superinfected line induces unidirectional cytoplasmic incompatibility (CI) when crossed to each single infected parental line, suggesting that the superinfection would have the capacity to replace either of the single constituent infections already present in a mosquito population. No significant differences in fitness parameters were observed between the superinfected line and the parental lines under the experimental conditions tested. Finally, the superinfected line blocks DENV replication more efficiently than the single wMel strain when challenged with blood meals from viremic dengue patients. These results suggest that the deployment of superinfections could be used to replace single infections and may represent an effective strategy to help manage potential resistance by DENV to field deployments of single infected strains.",
author = "Joubert, {D Albert} and Thomas Walker and Carrington, {Lauren B} and {Taneja De Bruyne}, Jyotika and Kien, {Duong Hue T} and {Le Thanh Hoang}, Nhat and Chau, {Nguyen Van Vinh} and Inaki Iturbe-Ormaetxe and Simmons, {Cameron P} and O'Neill, {Scott L}",
year = "2016",
doi = "10.1371/journal.ppat.1005434",
language = "English",
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Joubert, DA, Walker, T, Carrington, LB, Taneja De Bruyne, J, Kien, DHT, Le Thanh Hoang, N, Chau, NVV, Iturbe-Ormaetxe, I, Simmons, CP & O'Neill, SL 2016, 'Establishment of a Wolbachia superinfection in Aedes aegypti mosquitoes as a potential approach for future resistance management', PLoS Pathogens, vol. 12, no. 2, pp. 1-19. https://doi.org/10.1371/journal.ppat.1005434

Establishment of a Wolbachia superinfection in Aedes aegypti mosquitoes as a potential approach for future resistance management. / Joubert, D Albert; Walker, Thomas; Carrington, Lauren B; Taneja De Bruyne, Jyotika; Kien, Duong Hue T; Le Thanh Hoang, Nhat; Chau, Nguyen Van Vinh; Iturbe-Ormaetxe, Inaki; Simmons, Cameron P; O'Neill, Scott L.

In: PLoS Pathogens, Vol. 12, No. 2, 2016, p. 1-19.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - Establishment of a Wolbachia superinfection in Aedes aegypti mosquitoes as a potential approach for future resistance management

AU - Joubert, D Albert

AU - Walker, Thomas

AU - Carrington, Lauren B

AU - Taneja De Bruyne, Jyotika

AU - Kien, Duong Hue T

AU - Le Thanh Hoang, Nhat

AU - Chau, Nguyen Van Vinh

AU - Iturbe-Ormaetxe, Inaki

AU - Simmons, Cameron P

AU - O'Neill, Scott L

PY - 2016

Y1 - 2016

N2 - Wolbachia pipientis is an endosymbiotic bacterium estimated to chronically infect between 40–75% of all arthropod species. Aedes aegypti, the principle mosquito vector of dengue virus (DENV), is not a natural host of Wolbachia. The transinfection of Wolbachia strains such as wAlbB, wMel and wMelPop-CLA into Ae. aegypti has been shown to significantly reduce the vector competence of this mosquito for a range of human pathogens in the laboratory. This has led to wMel-transinfected Ae. aegypti currently being released in five countries to evaluate its effectiveness to control dengue disease in human populations. Here we describe the generation of a superinfected Ae. aegypti mosquito line simultaneously infected with two avirulent Wolbachia strains, wMel and wAlbB. The line carries a high overall Wolbachia density and tissue localisation of the individual strains is very similar to each respective single infected parental line. The superinfected line induces unidirectional cytoplasmic incompatibility (CI) when crossed to each single infected parental line, suggesting that the superinfection would have the capacity to replace either of the single constituent infections already present in a mosquito population. No significant differences in fitness parameters were observed between the superinfected line and the parental lines under the experimental conditions tested. Finally, the superinfected line blocks DENV replication more efficiently than the single wMel strain when challenged with blood meals from viremic dengue patients. These results suggest that the deployment of superinfections could be used to replace single infections and may represent an effective strategy to help manage potential resistance by DENV to field deployments of single infected strains.

AB - Wolbachia pipientis is an endosymbiotic bacterium estimated to chronically infect between 40–75% of all arthropod species. Aedes aegypti, the principle mosquito vector of dengue virus (DENV), is not a natural host of Wolbachia. The transinfection of Wolbachia strains such as wAlbB, wMel and wMelPop-CLA into Ae. aegypti has been shown to significantly reduce the vector competence of this mosquito for a range of human pathogens in the laboratory. This has led to wMel-transinfected Ae. aegypti currently being released in five countries to evaluate its effectiveness to control dengue disease in human populations. Here we describe the generation of a superinfected Ae. aegypti mosquito line simultaneously infected with two avirulent Wolbachia strains, wMel and wAlbB. The line carries a high overall Wolbachia density and tissue localisation of the individual strains is very similar to each respective single infected parental line. The superinfected line induces unidirectional cytoplasmic incompatibility (CI) when crossed to each single infected parental line, suggesting that the superinfection would have the capacity to replace either of the single constituent infections already present in a mosquito population. No significant differences in fitness parameters were observed between the superinfected line and the parental lines under the experimental conditions tested. Finally, the superinfected line blocks DENV replication more efficiently than the single wMel strain when challenged with blood meals from viremic dengue patients. These results suggest that the deployment of superinfections could be used to replace single infections and may represent an effective strategy to help manage potential resistance by DENV to field deployments of single infected strains.

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