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 in | PLoS neglected tropical diseases Vol. 7; no. 3; p. e2152 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
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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. |
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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 – sequence: 3 givenname: Cristina surname: Di Genua fullname: Di Genua, Cristina – sequence: 4 givenname: Anna-Bella surname: Failloux fullname: Failloux, Anna-Bella – sequence: 5 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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DocumentTitleAlternate | Wolbachia wMel in Aedes albopictus: Fitness & CHIKV |
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Keywords | Mosquitoes Wolbachia Chikungunya virus Chikungunya infection Dengue virus Fecundity Saliva Blood Animals Female Male Aedes Drosophila melanogaster Microbial Interactions |
Language | English |
License | Attribution: http://creativecommons.org/licenses/by 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 properly credited. Creative Commons Attribution License |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 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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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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