A Wolbachia wMel transinfection in Aedes albopictus is not detrimental to host fitness and inhibits Chikungunya virus

Wolbachia inherited intracellular bacteria can manipulate the reproduction of their insect hosts through cytoplasmic incompatibility (CI), and certain strains have also been shown to inhibit the replication or dissemination of viruses. Wolbachia strains also vary in their relative fitness effects on...

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Published inPLoS neglected tropical diseases Vol. 7; no. 3; p. e2152
Main Authors Blagrove, Marcus S C, Arias-Goeta, Camilo, Di Genua, Cristina, Failloux, Anna-Bella, Sinkins, Steven P
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.03.2013
Public Library of Science (PLoS)
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Abstract Wolbachia inherited intracellular bacteria can manipulate the reproduction of their insect hosts through cytoplasmic incompatibility (CI), and certain strains have also been shown to inhibit the replication or dissemination of viruses. Wolbachia strains also vary in their relative fitness effects on their hosts and this is a particularly important consideration with respect to the potential of newly created transinfections for use in disease control. In Aedes albopictus mosquitoes transinfected with the wMel strain from Drosophila melanogaster, which we previously reported to be unable to transmit dengue in lab challenges, no significant detrimental effects were observed on egg hatch rate, fecundity, adult longevity or male mating competitiveness. All these parameters influence the population dynamics of Wolbachia, and the data presented are favourable with respect to the aim of taking wMel to high population frequency. Challenge with the chikungunya (CHIKV) virus, for which Ae. albopictus is an important vector, was conducted and the presence of wMel abolished CHIKV dissemination to the saliva. Taken together, these data suggest that introducing wMel into natural Ae. albopictus populations using bidirectional CI could be an efficient strategy for preventing or reducing the transmission of arboviruses by this species.
AbstractList The tiger mosquito Aedes albopictus is an invasive disease vector whose range has expanded throughout the tropics, and some temperate regions, in recent decades from its native South East Asia. It is an important vector of human viruses including dengue and chikungunya; in recent years a mutation has been detected in chikungunya virus that specifically increases transmission efficiency by Ae. albopictus , causing concern that epidemics of this disease will become more widespread and severe. Here we show that when transinfected with a strain of the symbiont Wolbachia called w Mel, originating in fruitflies, the ability of the mosquito to transmit the mutated chikungunya virus was abolished in lab experiments. Furthermore, the w Mel strain was shown to produce no detectable fitness costs in this new host, examining numbers of eggs produced, egg hatch, lifespan, and male mating competitiveness compared to wildtypes. This is encouraging with respect to developing the system for use in the control of dengue and chikungunya viruses.
BACKGROUNDWolbachia inherited intracellular bacteria can manipulate the reproduction of their insect hosts through cytoplasmic incompatibility (CI), and certain strains have also been shown to inhibit the replication or dissemination of viruses. Wolbachia strains also vary in their relative fitness effects on their hosts and this is a particularly important consideration with respect to the potential of newly created transinfections for use in disease control. METHODOLOGY/PRINCIPAL FINDINGSIn Aedes albopictus mosquitoes transinfected with the wMel strain from Drosophila melanogaster, which we previously reported to be unable to transmit dengue in lab challenges, no significant detrimental effects were observed on egg hatch rate, fecundity, adult longevity or male mating competitiveness. All these parameters influence the population dynamics of Wolbachia, and the data presented are favourable with respect to the aim of taking wMel to high population frequency. Challenge with the chikungunya (CHIKV) virus, for which Ae. albopictus is an important vector, was conducted and the presence of wMel abolished CHIKV dissemination to the saliva. CONCLUSIONS/SIGNIFICANCETaken together, these data suggest that introducing wMel into natural Ae. albopictus populations using bidirectional CI could be an efficient strategy for preventing or reducing the transmission of arboviruses by this species.
  Background Wolbachia inherited intracellular bacteria can manipulate the reproduction of their insect hosts through cytoplasmic incompatibility (CI), and certain strains have also been shown to inhibit the replication or dissemination of viruses. Wolbachia strains also vary in their relative fitness effects on their hosts and this is a particularly important consideration with respect to the potential of newly created transinfections for use in disease control. Methodology/Principal Findings In Aedes albopictus mosquitoes transinfected with the wMel strain from Drosophila melanogaster, which we previously reported to be unable to transmit dengue in lab challenges, no significant detrimental effects were observed on egg hatch rate, fecundity, adult longevity or male mating competitiveness. All these parameters influence the population dynamics of Wolbachia, and the data presented are favourable with respect to the aim of taking wMel to high population frequency. Challenge with the chikungunya (CHIKV) virus, for which Ae. albopictus is an important vector, was conducted and the presence of wMel abolished CHIKV dissemination to the saliva. Conclusions/significance Taken together, these data suggest that introducing wMel into natural Ae. albopictus populations using bidirectional CI could be an efficient strategy for preventing or reducing the transmission of arboviruses by this species.
Wolbachia inherited intracellular bacteria can manipulate the reproduction of their insect hosts through cytoplasmic incompatibility (CI), and certain strains have also been shown to inhibit the replication or dissemination of viruses. Wolbachia strains also vary in their relative fitness effects on their hosts and this is a particularly important consideration with respect to the potential of newly created transinfections for use in disease control. In Aedes albopictus mosquitoes transinfected with the wMel strain from Drosophila melanogaster, which we previously reported to be unable to transmit dengue in lab challenges, no significant detrimental effects were observed on egg hatch rate, fecundity, adult longevity or male mating competitiveness. All these parameters influence the population dynamics of Wolbachia, and the data presented are favourable with respect to the aim of taking wMel to high population frequency. Challenge with the chikungunya (CHIKV) virus, for which Ae. albopictus is an important vector, was conducted and the presence of wMel abolished CHIKV dissemination to the saliva. Taken together, these data suggest that introducing wMel into natural Ae. albopictus populations using bidirectional CI could be an efficient strategy for preventing or reducing the transmission of arboviruses by this species.
Background: Wolbachia inherited intracellular bacteria can manipulate the reproduction of their insect hosts through cytoplasmic incompatibility (CI), and certain strains have also been shown to inhibit the replication or dissemination of viruses. Wolbachia strains also vary in their relative fitness effects on their hosts and this is a particularly important consideration with respect to the potential of newly created transinfections for use in disease control. Methodology/Principal Findings: In Aedes albopictus mosquitoes transinfected with the wMel strain from Drosophila melanogaster, which we previously reported to be unable to transmit dengue in lab challenges, no significant detrimental effects were observed on egg hatch rate, fecundity, adult longevity or male mating competitiveness. All these parameters influence the population dynamics of Wolbachia, and the data presented are favourable with respect to the aim of taking wMel to high population frequency. Challenge with the chikungunya (CHIKV) virus, for which Ae. albopictus is an important vector, was conducted and the presence of wMel abolished CHIKV dissemination to the saliva. Conclusions/significance: Taken together, these data suggest that introducing wMel into natural Ae. albopictus populations using bidirectional CI could be an efficient strategy for preventing or reducing the transmission of arboviruses by this species.
Background: Wolbachia inherited intracellular bacteria can manipulate the reproduction of their insect hosts through cytoplasmic incompatibility (CI), and certain strains have also been shown to inhibit the replication or dissemination of viruses. Wolbachia strains also vary in their relative fitness effects on their hosts and this is a particularly important consideration with respect to the potential of newly created transinfections for use in disease control.Methodology/Principal FindingsIn Aedes albopictus mosquitoes transinfected with the wMel strain from Drosophila melanogaster, which we previously reported to be unable to transmit dengue in lab challenges, no significant detrimental effects were observed on egg hatch rate, fecundity, adult longevity or male mating competitiveness. All these parameters influence the population dynamics of Wolbachia, and the data presented are favourable with respect to the aim of taking wMel to high population frequency. Challenge with the chikungunya (CHIKV) virus, for which Ae. albopictus is an important vector, was conducted and the presence of wMel abolished CHIKV dissemination to the saliva.Conclusions/significanceTaken together, these data suggest that introducing wMel into natural Ae. albopictus populations using bidirectional CI could be an efficient strategy for preventing or reducing the transmission of arboviruses by this species.
Wolbachia inherited intracellular bacteria can manipulate the reproduction of their insect hosts through cytoplasmic incompatibility (CI), and certain strains have also been shown to inhibit the replication or dissemination of viruses. Wolbachia strains also vary in their relative fitness effects on their hosts and this is a particularly important consideration with respect to the potential of newly created transinfections for use in disease control.In Aedes albopictus mosquitoes transinfected with the wMel strain from Drosophila melanogaster, which we previously reported to be unable to transmit dengue in lab challenges, no significant detrimental effects were observed on egg hatch rate, fecundity, adult longevity or male mating competitiveness. All these parameters influence the population dynamics of Wolbachia, and the data presented are favourable with respect to the aim of taking wMel to high population frequency. Challenge with the chikungunya (CHIKV) virus, for which Ae. albopictus is an important vector, was conducted and the presence of wMel abolished CHIKV dissemination to the saliva.Taken together, these data suggest that introducing wMel into natural Ae. albopictus populations using bidirectional CI could be an efficient strategy for preventing or reducing the transmission of arboviruses by this species.
Audience Academic
Author Failloux, Anna-Bella
Sinkins, Steven P
Blagrove, Marcus S C
Di Genua, Cristina
Arias-Goeta, Camilo
AuthorAffiliation 2 Institut Pasteur, Department of Virology, Paris, France
Monash University, Australia
1 University of Oxford, Peter Medawar Building for Pathogen Research and Departments of Medicine (NDM)/Zoology, Oxford, United Kingdom
AuthorAffiliation_xml – name: 1 University of Oxford, Peter Medawar Building for Pathogen Research and Departments of Medicine (NDM)/Zoology, Oxford, United Kingdom
– name: 2 Institut Pasteur, Department of Virology, Paris, France
– name: Monash University, Australia
Author_xml – sequence: 1
  givenname: Marcus S C
  surname: Blagrove
  fullname: Blagrove, Marcus S C
  organization: University of Oxford, Peter Medawar Building for Pathogen Research and Departments of Medicine (NDM)/Zoology, Oxford, United Kingdom
– sequence: 2
  givenname: Camilo
  surname: Arias-Goeta
  fullname: Arias-Goeta, Camilo
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  givenname: Cristina
  surname: Di Genua
  fullname: Di Genua, Cristina
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  givenname: Anna-Bella
  surname: Failloux
  fullname: Failloux, Anna-Bella
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  givenname: Steven P
  surname: Sinkins
  fullname: Sinkins, Steven P
BackLink https://www.ncbi.nlm.nih.gov/pubmed/23556030$$D View this record in MEDLINE/PubMed
https://pasteur.hal.science/pasteur-01680359$$DView record in HAL
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ContentType Journal Article
Copyright COPYRIGHT 2013 Public Library of Science
Attribution
2013 Blagrove et al 2013 Blagrove et al
2013 Blagrove et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Blagrove MSC, Arias-Goeta C, Di Genua C, Failloux A-B, Sinkins SP (2013) A Wolbachia wMel Transinfection in Aedes albopictus Is Not Detrimental to Host Fitness and Inhibits Chikungunya Virus. PLoS Negl Trop Dis 7(3): e2152. doi:10.1371/journal.pntd.0002152
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– notice: 2013 Blagrove et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Blagrove MSC, Arias-Goeta C, Di Genua C, Failloux A-B, Sinkins SP (2013) A Wolbachia wMel Transinfection in Aedes albopictus Is Not Detrimental to Host Fitness and Inhibits Chikungunya Virus. PLoS Negl Trop Dis 7(3): e2152. doi:10.1371/journal.pntd.0002152
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DocumentTitleAlternate Wolbachia wMel in Aedes albopictus: Fitness & CHIKV
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Issue 3
Keywords Mosquitoes
Wolbachia
Chikungunya virus
Chikungunya infection
Dengue virus
Fecundity
Saliva
Blood
Animals
Female
Male
Aedes
Drosophila melanogaster
Microbial Interactions
Language English
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PMCID: PMC3610642
Conceived and designed the experiments: MSCB SPS ABF. Performed the experiments: MSCB CAG CDG. Analyzed the data: MSCB ABF SPS. Wrote the paper: MSCB SPS.
The authors have declared that no competing interests exist.
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Snippet Wolbachia inherited intracellular bacteria can manipulate the reproduction of their insect hosts through cytoplasmic incompatibility (CI), and certain strains...
Background: Wolbachia inherited intracellular bacteria can manipulate the reproduction of their insect hosts through cytoplasmic incompatibility (CI), and...
BACKGROUNDWolbachia inherited intracellular bacteria can manipulate the reproduction of their insect hosts through cytoplasmic incompatibility (CI), and...
The tiger mosquito Aedes albopictus is an invasive disease vector whose range has expanded throughout the tropics, and some temperate regions, in recent...
  Background Wolbachia inherited intracellular bacteria can manipulate the reproduction of their insect hosts through cytoplasmic incompatibility (CI), and...
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StartPage e2152
SubjectTerms Aedes
Aedes - microbiology
Aedes - physiology
Aedes - virology
Animals
Chikungunya fever
Chikungunya virus
Chikungunya virus - growth & development
Dengue fever
Development and progression
Drosophila melanogaster
Drosophila melanogaster - microbiology
Experiments
Female
Health aspects
Host-parasite relationships
Insects
Life Sciences
Male
Males
Mathematical models
Medicine
Microbial Interactions
Microbiology and Parasitology
Mosquitoes
Mutation
Physiological aspects
Saliva
Saliva - virology
Virology
Viruses
Wolbachia
Wolbachia - growth & development
Wolbachia - isolation & purification
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Title A Wolbachia wMel transinfection in Aedes albopictus is not detrimental to host fitness and inhibits Chikungunya virus
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